National Academies Press: OpenBook

Biosolids Applied to Land: Advancing Standards and Practices (2002)

Chapter: 6 Evaluation of EPA's Approach to Setting Pathogen Standards

« Previous: 5 Evaluation of EPA's Approach to Setting Chemical Standards
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

6
Evaluation of EPA’s Approach to Setting Pathogen Standards

Treatment of domestic sewage sludge is required to minimize the risk of adverse health effects from pathogens in biosolids applied to land. In 1993, EPA published regulations establishing the processes and conditions it deemed necessary to minimize these risks. Unlike the chemical standards, the pathogen regulations are not risk-based standards but are operational standards intended to reduce the presence of pathogens to concentrations that are not expected to cause adverse health effects. The standards include treatment requirements, site restrictions, and monitoring requirements.

This chapter reviews the pathogen standards for land-applied biosolids in light of current knowledge of the potential pathogens in biosolids, how humans might be exposed to those pathogens, and factors that affect exposure (environmental fate, regional variations, and host factors). It also reviews approaches for conducting microbial risk assessments and discusses how those approaches might be used to improve EPA’s pathogens standards for biosolids. This chapter does not review health effects studies (see Chapter 3).

PATHOGEN STANDARDS

EPA established two categories of biosolids: Class A biosolids, which have no detectable concentrations of pathogens, and Class B biosolids, which have detectable concentrations of pathogens. With the goal of providing

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

equivalent levels of public-health protection from pathogen exposure, EPA applied different use restrictions to each biosolids category.

Class B Requirements

A combination of treatment and site restrictions for Class B biosolids are intended to result in a reduction of pathogenic and indicator microorganisms (certain species of organisms believed to indicate the presence of a larger set of pathogens) to undetectable concentrations prior to public contact (Southworth 2001). Bulk biosolids applied to land must meet both treatment and use requirements (40 CFR 503.15[a]). EPA (1993) recognizes that those requirements do not necessarily consider risks to workers applying the biosolids at a site.

Treatment Requirements

Class B biosolids must be treated to meet one of three criteria: a fecal coliform count of less than 2×106/gram (g) of dry solids at the time of disposal, treatment by a process to significantly reduce pathogens (PSRP), or treatment by a process that is equivalent to a PSRP. In the 1993 regulations, five processes were listed as PSRPs (and thus sufficient to meet the Class B treatment requirements):

  1. Aerobic digestion at defined time and temperature combinations.

  2. Air drying for 3 months, with at least 2 months at average ambient daily temperatures above freezing.

  3. Anaerobic digestion under defined time and temperature conditions.

  4. Composting under defined time and temperature conditions.

  5. Lime stabilization so that the pH is greater than 12 after 2 h of contact.

These PSRPs were selected because they result in fecal-coliform concentrations of less than 2×106/g of dry solids, and they reduce Salmonella and enteric virus concentrations by a factor of 10 (EPA 1999).

The third treatment criterion requires that the permit authority approve the processes being used as equivalent to a PSRP. In practice, permit authorities have relied on the recommendations of the EPA Pathogen Equivalency Committee (PEC) (Cook and Hanlon 1993) when determining whether a particular treatment system should be designated PSRP. As of October 1999, PEC had recommended that two additional processes be designated PSRPs.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Site Restrictions

The site restrictions for Class B biosolids (listed in Box 6–1) were developed on the basis of the time attenuation required to reduce the levels of pathogens (bacteria, viruses, and helminths) to below detectable concentrations at the time of public exposure (equivalent to those achieved by Class A biosolids) (Southworth 2001). The use restrictions correspond to important exposure pathways (Table 6–1).

Several potential exposure routes do not appear to have been considered when those use restrictions were developed. For example, inhalation of dust was presumed to occur only on-site, and controlling access to the site was intended to prevent such inhalation. The potential for off-site exposure to wind-blown dust and aerosols does not appear to have been considered. Nor was the potential transport of pathogens in runoff from the site to neighboring properties considered.

In addition, regulations require that public access to the site be restricted for either 30 days or 1 year, depending on the probability of public exposure. This restriction is vague, however, and has been interpreted by some state agencies as a requirement for posting warnings but not necessarily providing access barriers. In other contexts, such as municipal solid-waste landfills, EPA has been more specific about access controls, “Owners or operators [of landfills] must control public access…by using artificial barriers, natural barriers or both, as appropriate to protect human health and the environment” (40 CFR 258.25). Furthermore, there is no requirement that on-site measurements be taken to confirm that the treatment and site restrictions for Class B biosolids result in pathogens concentrations below detection.

Class A Requirements

For biosolids to be categorized as Class A with respect to pathogens, they must meet one of six criteria:

  1. Time and temperature requirements based on percentage of solids in the material.

  2. pH adjustment accompanied by high temperature and solids drying.

  3. Monitoring of enteric viruses and helminths after a treatment process to ensure below-detection concentrations.

  4. Monitoring of enteric viruses and helminths in the biosolids at the time they are distributed or applied to land.

  5. Treatment by a process for the further reduction of pathogens (PFRP).

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

BOX 6–1 Site Restrictions for Class B Biosolids

  • Food crops with harvested parts that touch the biosolids/soil mixture and are totally above the land surface shall not be harvested for 14 months after application of biosolids.

  • Food crops with harvested parts below the surface of the land shall not be harvested for 20 months after application of biosolids when the biosolids remain on the land surface for four months or longer prior to incorporation into the soil.

  • Food crops with harvested parts below the surface of the land shall not be harvested for 38 months after application of biosolids when the biosolids remain on the land surface for less than four months prior to incorporation into the soil.

  • Food crops, feed crops, and fiber crops shall not be harvested for 30 days after application of biosolids.

  • Animals shall not be grazed on the land for 30 days after application of biosolids.

  • Turf grown on land where biosolids is applied shall not be harvested for one year after application of the biosolids when the harvested turf is placed on either land with a high potential for public exposure or a lawn, unless otherwise specified by the permitting authority.

  • Public access to land with a high potential for public exposure shall be restricted for one year after application of biosolids.

  • Public access to land with a low potential for public exposure shall be restricted for 30 days after application of biosolids.

Source: Adapted from 40 CFR 503.32(b)(5).

  1. Treatment in a process deemed equivalent to a PFRP. There are seven processes that are designated PFRPs for Class A biosolids: (a) composting with minimum time and temperature conditions, (b) heat drying with specified temperature and moisture conditions, (c) high-temperature heat treatment (no moisture content condition), (d) thermophilic aerobic digestion at specified time and temperature, (e) beta irradiation at specified dosage, (f) gamma irradiation at specified dosage, and (g) pasteurization. As with Class B biosolids, PEC has the authority to recommend to permit authorities that additional processes be designated PFRP. As of October 1999, nine additional processes were granted PFRP status by PEC (EPA 1999).

The goal of the treatment processes to achieve Class A biosolids is to reduce pathogen densities to below the following detection limits for these organisms: less than 3 most probable number (MPN) per 4 g of total solids for Salmonella sp.; less than 1 plaque-forming unit (PFU) per 4 g of total solids

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

TABLE 6–1 Pathways of Exposure and Applicable Use Restrictions (Class B Biosolids Only)

Pathways

Part 503 Required Use Restriction

Handling soil from fields where biosolids have been applied

No public accessa to application until at least 1 year after Class B biosolids application

Handling soil or food from home gardens where biosolids have been applied

Class B biosolids may not be applied on home gardens

Inhaling dustb

No public access to application sites until at least 1 year after Class B biosolids application

Walking through fields where biosolids have been appliedb

No public access to fields until at least 1 year after Class B biosolids application

Consuming crops from fields on which biosolids have been applied

Site restrictions that prevent the harvesting of crops until environmental attenuation has taken place.

Consuming milk or animal products from animals grazing on fields where biosolids have been applied

No animal grazing for 30 days after Class B biosolids have been applied

Ingesting surface water contaminated by runoff from fields where biosolids have been applied

Class B biosolids may not be applied within 10 meters of any waters to prevent runoff from biosolids-amended land

Ingesting inadequately cooked fish from water contaminated by runoff from fields where biosolids have been applied, affecting the surface water

Class B biosolids may not be applied with 10 meters of any waters prevent runoff from biosolids-amended land

Contact with vectors that have been in contact with biosolids

All land-applied biosolids must meet one of the vector-attraction-reduction options

aPublic-access restrictions do not apply to farm workers. If there is low probability of public exposure to an application site, the public-access restrictions apply for only 30 days. However, application sites that are likely to be accessed by the public, such as ballfields, are subject to 1-year public-access restrictions.

bAgricultural land is private property and not considered to have a high potential for public access. Nonetheless, public-access restrictions are applied.

Source: Adapted from EPA 1999.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

for enteric viruses; and less than 1 viable ova per 4 g of total solids for helminths. When the Part 503 regulations were developed, Class A certification was generally based on the presence of either Salmonella or fecal coliforms (indicator bacteria) (Southworth 2001), because only a few laboratories were capable of conducting virus and helminth analyses and more time was required for these analyses (2–4 weeks). Since then, the number of laboratories capable of such analyses has increased dramatically, and analysis time has decreased.

Class A pathogens requirements must be met before or at the same time that vector-attraction reduction requirements are met. For any criteria, the microbial agents are measured when the biosolids are used, disposed of, or prepared for distribution. At that time, Class A biosolids must meet one of two requirements: either the density of fecal coliforms is less than 1,000 MPN per gram of total solids or the density of Salmonella sp. is less than 3 MPN per 4 g of total solids.

EPA’s Approach to Assessing Microbial Risks

The Part 503 standards for pathogens were not developed using a risk-based framework, nor were they intended to be. In 1989, the Cooperative State Research Service Technical Committee W-170 (1989) reviewed the proposed Part 503 standards and stated, ”There is some concern regarding EPA’s treatment of pathogens. While it was stated that the state of the art was such that a risk assessment for pathogens was not possible, we feel that this point was glossed over rather quickly and needs greater justification.” The W-170 committee also noted that EPA was developing risk-based criteria for exposure to viruses in drinking water at the time of the proposed Part 503 standards.

A few years before the Part 503 rule was proposed, EPA stated the following (Venosa 1985) on the use of PSRPs for the operative Part 257 sewage sludge regulations:

For a sludge treatment process to qualify as a ‘process to significantly reduce pathogens’ (PSRP), it must produce a pathogen reduction equivalent to that obtained by a good anaerobic digestion. The logic of the definition rests on the observation that agricultural use of anaerobically digested sludge as a fertilizer has been practiced for many years with no evidence that the practice has caused human illness, provided that the digestion is adequate. Since these farming operations were on land with limited access and clearly defined use, this same restriction was applied to the use of PSRP sludge. Unfortu-

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

nately, this definition is not based on sound scientific information related to the survival and transport of pathogens in sludge amended soils. Further, the paucity of documented health problems associated with the land application of sludge may reflect the lack of sufficiently sensitive epidemiological tools to detect small scale incidents of disease.

The committee notes, however, that the lack of such studies does not suggest that there is a risk from pathogens.

The lack of a risk-assessment approach means that there is no explicit delineation of acceptable risk concentrations for Class A or Class B biosolids in the Part 503 rule. Before promulgation of the regulations, EPA funded development of preliminary risk assessments for exposure to parasites (EPA 1991a), bacteria (EPA 1991b), and viruses (EPA 1992) in biosolids. However, it is not clear to what extent these preliminary assessments were used in the development or revision of the Part 503 rule. The exposure assessments would be useful for more substantial risk-assessment development.

Although a risk-based approach might have been problematic when the Part 503 rule was proposed, it is clearly an appropriate approach to use at present. A risk-based approach to assessing pathogens in biosolids offers several distinct advantages over the present framework. First, a risk-based approach would help to address the lack of sufficient epidemiological study of microbial risk from biosolids exposure. See Chapter 3 for discussion of the need for more epidemiological investigation.

Second, as noted by Venosa (1985), the fundamental basis of biosolids regulations with respect to protection against pathogens rests on the assertion that, historically, agricultural use of anaerobically digested biosolids on fields (with protection from public access) results in no discernable human health effects. In promulgating the Part 503 rule for pathogens, EPA made a judgment that the treatment and disposal practices for Class A and Class B biosolids provided public-health protection equal to that of the traditional use of anaerobically digested biosolids. That judgment was in effect an implicit risk assessment. If EPA performed an explicit risk assessment, the levels of public-health protection for Class A and Class B biosolids could be more consistently compared.

Third, EPA explicitly excluded risk to on-site workers from its consideration of appropriate levels of treatment. This exclusion might be particularly important for Class B biosolids, which have less stringent treatment before land application. In addition, EPA did not consider the potential for airborne and waterborne release and dispersal of microorganisms for off-site exposure (although it did consider the potential for on-site exposure to microorgan-

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

isms). The use of a risk-assessment approach can allow a systematic consideration of these pathways.

Fourth, the basis for the EPA definitions of Class A biosolids relies on a numeric fecal coliform or Salmonella standard and a below-detection standard for viruses and helminths in a defined amount of biosolids (criteria 3 and 4). EPA reasoned that the combination of Class B treatment requirements and site-management restrictions resulted in an acceptable level of public-health protection. The use of below-detection criteria in some defined amount of biosolids originates from the use of a particular sample size in analysis (for logistical reasons). The absence of microorganisms in a small amount of material does not ensure that microorganisms are absent in a larger sample from the same source. In addition, as has been suggested in the case of re-use of wastewater for agricultural purposes, a below-detection standard might be unnecessarily stringent (Blumenthal et al. 2000). A risk-assessment approach can establish numerical limits to achieve a defined level of human health risk.

Evaluation of Operational Standards

Techniques for Reducing Pathogens

As discussed above and in Chapter 2, techniques that combine physical, chemical, and biological processes are used to optimize pathogen reduction in biosolids. Two of the physical factors for reduction are heating and cavitation. It is difficult to examine the impact of only one physical factor, such as temperature, on reduction. Some studies have isolated temperature effects on Ascaris egg inactivation. Table 6–2 gives predicted detention times for complete (100%) inactivation of Ascaris eggs at different temperatures (Mbela 1988). At 52°C, complete inactivation of the eggs requires approximately 20 days. Inactivation with thermophilic alkaline processes and composting of biosolids requires approximately 3 to 5 days. Inactivation will also be affected by other factors such as ammonia, organic constituents, dissolved solids, and hydroxide anions (Evans and Puskas 1986; Reimers et al. 1986a).

Cavitation processes are also used to inactivate resistant microorganisms. Cavitation is a term for processes that impart high mechanical energy to a fluid, resulting in local transient microzones of high temperature and pressure. Full-scale installation of such systems has not been done. However, cavitation processes, such as ultrasound or pulse power, have inactivated protozoan oocysts and assisted in enhancing anaerobic digestion processes (Reimers et al. 1985; Arrowood 1995; Patel 1996).

Chemical disinfection of biosolids has been used for over 50 years. The chemicals are classified on the basis of the mode of disinfection and stabiliza-

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

TABLE 6–2 Detention Times for Complete Inactivation of Ascaris Eggs in Aerobic and Anaerobic Digestion Processes

 

Detention Time

Temperature(°C)

Aerobic Digestion

Anaerobic Digestion

25

130 d

74 d

35

90 d

53 d

45

50 d

30 d

55

10 d

9 d

57

2 d

4 d

58

<1 h

3 d

59

<1 h

12 h

60

<1 h

<1 h

70

<1 h

<1 h

 

Source: Mbela 1988. Reprinted with permission from the author.

tion (see Table 6–3). At present, only alkaline stabilization is used on a large-scale basis. Alkaline stabilization agents include lime, cement kiln dust, Portland cement, and alkaline fly ash (C-fly ash). Alkaline stabilization processes produce Class B biosolids. To yield Class A biosolids, increased temperatures or ammonia are necessary to inactivate highly resistant viruses, protozoan spores, and helminth eggs. Alkaline processes coupled with increased temperature yield a stable Class A product within 3 days. By increasing the temperature to 50°C, the effectiveness of ammonia and noncharged ammonia is increased by 5-fold and 10-fold, respectively (Bujoczek 2001). Yang (1996) confirmed this interrelationship (Table 6–4). As the solids content of the biosolids increases, the effectiveness of the alkaline disinfection increases (Yang 1996). Acid trimming enhances the exothermic reaction, because the acids generally release 10 times more heat than pulverized quicklime.

Biological processing has been effective in the digesting, composting, and storage of biosolids. In these processes, there is mechanical or autothermal heating. Biocidal inactivation has been observed in lagoon storage. Anaerobic biosolids required 40% less inactivation time than aerobic biosolids, although above 50–55°C, thermal inactivation is predominant. Furthermore, as the solids content of anaerobic biosolids increases, the inactivation rates increase. An increase in solids from 4% to 24% resulted in a 5-fold increase in parasite and bacteria die-off and a 25-fold increase in virus die-off. Soils tend to reduce the rate of die-off of parasites and viruses by 3 to 5 times in nontreated

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

TABLE 6–3 Chemicals Used for Disinfecting Biosolids

Alkaline Agents

Acid Trimming Agents

ORP Controlling Agents

Noncharged Disinfectants

Lime

Cement kiln dust

Sulfuric acid

Nitric acid

Ozone

Peroxide

Ammonia (alkaline treatment)

Portland cement alkaline Fly ash

Phosphoric acid

sulfamic acid

 

Amines (alkaline treatment and composting)

Silicates

Spent bauxite hydroxide anions

 

Organic acids, aldehydes, and ketones (anaerobic digestion and composting)

 

Nitrous acid (acidic treatment)

Abbreviation: ORP, oxidation reduction potential

Source: Reimers et al. 1999. Reprinted with permission from the author.

or lagoon-stored biosolids (Reimers et al. 2001). The impacts of pathogen inactivation factors on biosolids processing are shown in Table 6–5.

Reliability of Processes

In assessing the risk associated with biosolids management, the reliability of the treatment processes is important to consider, because adverse effects might result from a single exposure to an infectious agent. Reliability may be defined as the frequency (or probability) at which a certain concentration or lower of a pathogen is attained in the effluent of a process. To assess the risk distribution from pathogen disinfection processes, data collection is required.

As an example, Figure 6–1 presents the probability distribution for virus and helminth counts in raw sewage sludge at the Metropolitan Water Reclamation District of Greater Chicago (Lue-Hing et al. 1998). The treatment sequence included anaerobic digestion, dewatering, and long-term lagoon storage. All treated virus samples were below detection. The data are plotted using a Kaplan-Meir approach to impute values for the below-detection samples. For example, in the finished solids, 95% of the time the helminth concentrations were below 0.05 organisms per 4 g of solids.

In setting standards, both the typical (e.g., mean) performance and the proportion of time that a specific numerical level is exceeded are appropriate

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

TABLE 6–4 Relationship Between Ammonia Concentration and Temperature in Ascaris Inactivation

 

Ammonia Dosage for Ascaris Inactivation (days)

Temperature

0.1%

1.0%

4.0%

25°C

180

10

<1

35°C

10

3

<1

52°C

<1

<1

<1

 

Source: Data from Yang 1996.

metrics to be considered. For example, EPA-recommended water-quality criteria for micoorganisms in recreational waters are specified according to geometric mean levels (over 7 d) and not-to-exceed levels. No such metrics have been established for pathogens in biosolids.

Reliability of Use Controls

For Class B biosolids, use requirements (described earlier in Box 6–1) are relied on as impediments to exposure, at least for the general public. The resulting risk reductions can be assessed if the pathogen die-off rates are known and if the degree to which the use controls prevent exposure are known. Unfortunately, the reliability of these controls has not been studied on a systematic basis.

PATHOGENS IN BIOSOLIDS

Four major types of human pathogens can be found in biosolids: bacteria, viruses, protozoa, and helminths. EPA reviewed a broad spectrum of these agents in establishing its biosolids standards. Some of the principal pathogens considered by EPA are listed in Box 6–2. Since the development of the Part 503 rule, many new pathogens have been recognized, and the importance of others has increased. A selection of these pathogens are discussed below. It must be noted that despite the ability to isolate pathogens from raw sewage sludge and partially and fully treated biosolids, the mere isolation of pathogens does not in and of itself indicate that a risk exists. There are no scientifically documented outbreaks or excess illnesses that have occurred from microorganisms in treated biosolids. As will be discussed in detail later, risk is a function of the level of exposure, not simply the occurrence of an organism per se.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

TABLE 6–5 Parameters for Pathogen Inactivation in Biosolids

Biosolids Disinfection Process

Irradiation

Temperature

Solids Content

NH3

Organic By-Products

Desiccants

Composting

-

+

-

±

+

-

Anaerobic digestion

-

+

+

-

+

-

Aerobic digestion

-

+

+

-

-

-

Lagoon storage

-

+

+

-

+

-

Air drying

+

+

+

-

-

+

Alkaline stabilization

-

+

+

+

-

+

Irradiation

+

-

-

-

-

-

Note: +, the effect of the parameters in the column heads is to increase the rate or extent of inactivation in the process in column 1;–, the effect of these parameters do not influence the inactivation process.

Sources: Reimers et al. 1986a, 1999; Yang 1996; Rohwer 1984.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

FIGURE 6–1 Virus and helminths in raw and treated sludge at the Metropolitan Water Reclamation District of Greater Chicago. Source: Lue-Hing et al. 1998.

Viral Pathogens

More than 140 enteric viruses can be transmitted by biosolids. The caliciviruses, adenoviruses, hepatitis A and E viruses, astroviruses, and rotaviruses are of particular concern. These viruses are discussed below, but it must be emphasized that there are other viruses of potential health concern in biosolids.

Caliciviruses

Caliciviruses infect both humans and animals, but no evidence suggests that they infect across species. Human caliciviruses have been divided into two genera—the Norwalk viruses and the Sapporo viruses (Green et al. 2000). These viruses are believed to be a major cause of viral gastroenteritis (Deneen et al. 2000; Monroe et al. 2000) and are common causes of foodborne and waterborne disease. Little is known about the occurrence and environmental fate of these viruses because they cannot be grown in cell culture. Methods using polymerase chain reaction (PCR) are available for their detection in environmental samples, but a viability assay is not available (Huang et al.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

BOX 6–2 Principal Pathogens of Concern in Domestic Sewage and Sewage Sludge Considered in Establishing the Part 503 Rule

Bacteria

Salmonella sp.

Shigella sp.

Yersinia sp. Vibrio cholerae

Campylobacter jejuni

Escherichia coli

Enteric Viruses

Hepatitis A virus

Adenovirus

Norwalk virus

Caliciviruses

Rotaviruses

Enteroviruses

-Polioviruses

-Coxsackieviruses

-Echoviruses

Reoviruses

Astroviruses

Protozoa

Cryptosporidium

Entamoeba histolytica

Giardia lamblia

Balantidium coli

Toxoplasma gondii

Helminth Worms

Ascaris lumbricoides

Ascaris suum

Trichuris trichirua

Toxocara canis

Taenia saginata

Taenia solium

Necator americanus

Hymenolepis nana

Source: Adapted from EPA 1999.

2000). Feline caliciviruses (FCV) and a primate calicivirus (PAN-1) can be grown in cell culture and have been used as models for human calicivirus survival and removal by water-treatment processes (Dawson et al. 1993).

Adenoviruses

Adenoviruses are one of the most common and persistent viruses detected in wastewater (Enriquez et al. 1995). They are heat resistant Enteric adenoviruses have been detected in Class B biosolids (Sabalos 1998), and adenovirus type 40 has been detected in anaerobically digested biosolids. Some adenoviruses cause primarily respiratory diseases, and others appear to be only enteric pathogens. They are a common cause of diarrhea and respiratory infections in children. In immunosuppressed cancer patients, enteric adenoviruses cause serious infections, resulting in case fatalities of up to 50% (Gerba et al. 1996). Adenoviruses have been transmitted by recreational and drinking waters (Kukkula et al. 1997; Papapetropoulou and Vantarakis 1998).

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Hepatitis A and E Viruses

These viruses are now classified as two distinct groups of picornaviruses. Hepatitis E has caused major waterborne-disease outbreaks in developing countries but is not believed to be a serious problem in the United States. It has been reported to grow in cell culture (Wei et al. 2000). Hepatitis A has long been known to be transmitted by food and water, but no work has been done on its occurrence in biosolids. Cell-culture methods are available for its growth in the laboratory and detection in the environment. It is very stable at high temperatures (Croci et al. 1999) and has prolonged survival in the environment (Enriquez et al. 1995).

Astroviruses and Rotaviruses

Astroviruses are a cause of gastroenteritis primarily in children and have been associated with foodborne and waterborne outbreaks. They have been detected in water, wastewater, and more recently, in biosolids (Chapron et al. 2000). Rotaviruses are a leading cause of gastroenteritis in children and a major cause of hospitalization of children in the United States (Gerba et al. 1996). Rotaviruses are responsible for waterborne and foodborne outbreaks in the United States. They have been detected in wastewater, but few data are available on their occurrence in biosolids. Rotaviruses are the only double-stranded RNA viruses transmitted through water to humans. Both astroviruses and rotaviruses can be grown in cell culture.

Bacterial Pathogens

Escherichia coli 0157:H7

Several types of E. coli are pathogenic to human. Enterohaemorrhagic E. coli of the serotype 0157:H7 has been of the greatest concern in the United States. Exposure to contaminated drinking water, recreational water, and food has resulted in numerous outbreaks of diarrhea and, in some cases, mortality in young children because of hemolytic uremic syndrome. Exposure to both human and animal wastes have been associated with outbreaks (Rice 1999). Many of the outbreaks have resulted in some mortality. E. coli 0157:H7 occurs in domestic wastewater and has been detected in biosolids (Lytle et al. 1999). Because E. coli is common in biosolids and has the potential for regrowth (Pepper et al. 1993), it is important to assess its survival in biosolids. A quan-

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

titative risk-assessment model is available to assess the risk of infection from exposure to this pathogen (Haas et al. 2000).

Listeria montocytogenes

L. montocytogenes is primarily a foodborne pathogen that causes an invasive disease in immunocompromised people. It has a predilection for pregnant women and has potentially lethal consequences for the fetus and the newborn. Animals are also infected by the organism. Transmission of the organism has been linked to the use of biosolids on agricultural land, potentially contaminating crops and domestic animals. L. montocytogenes has been detected frequently in sewage sludge and in inactivated and anaerobically digested biosolids (Watkins and Sleath 1981; De Luca et al. 1998). For that reason, De Luca et al. (1998) suggested that biosolids not be applied to vegetable crops. Crop contamination was observed in Iraq where sewage-sludge cake was applied (Al-Ghazali and Al-Azawi 1990). A risk-assessment model is available to evaluate the health risks associated with L. montocytogenes in contaminated food (Lindqvist and Westoo 2000).

Helicobacter pylori

H. pylori is a major cause of stomach ulcers in humans and is associated with an increased risk of stomach cancer. Epidemiological evidence indicates that contaminated water and uncooked foods, particularly vegetables irrigated with untreated wastewater, are associated with increased risk of infection (Brown 2000). No culture methods are available for its detection in the environment. Molecular methods are available to determine its occurrence but not its viability (Hegarty et al. 1999).

Legionella spp.

Legionella spp. are associated with a potentially life-threatening respiratory illness in older people. Legionella is also associated with a milder fever and flulike illness called Pontiac fever. Outbreaks usually occur following the growth of the organism in cooling towers of buildings or thermally heated water. However, outbreaks also have been associated with composted potting mixes (Okazaki et al. 1998). Recently, an outbreak of Pontiac fever was reported among sewage treatment plant workers repairing a decanter for sewage

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

sludge concentration (Gregersen et al. 1999). Positive antibody titers to L. pneumophilia were found in all the ill workers, and high concentrations were isolated from biosolids. Legionella has been detected in aerosols at sewage treatment plants (Stampi et al. 2000). Legionella spp. will grow at temperatures of 40°C, and survival at higher temperatures is possible. Methods are available for its detection in environmental samples.

Staphylococcus aureus

Speculation has arisen about the possibility of S. aureus illness from land-applied biosolids. Although not always considered normal human microflora, S. aureus is nonetheless found on the skin of a large number of people (Voss 1975; Welbourn et al. 1976; McGinley el al. 1988; Noble 1998). Some skin conditions associated with this bacteria include atopic dermatitis, a superficial inflammation of the skin (Nishijima et al. 1995). It is uncertain whether S. aureus has a specific pathogenic role in atopic dermatitis or whether its presence represents an opportunistic colonization at a site rendered more susceptible by an underlying condition, thus complicating the clinical management of this condition (Lever 1996). Eczema is another inflammatory skin condition that may have a bacterial link. Eczema is characterized by redness, itching, and oozing lesions that can become scaly, crusted, or hardened. Increased severity and spreading of the condition has been associated with a cytotoxic effect of antibacterial antibody and complement reacting with bacterial antigens on skin cells (Welbourn et al. 1976).

It is possible that Staphylococcus is present in raw wastewater as a result of washing and personal hygiene. Indeed, Casanova et al. (2001) found S. aureus in graywaters from households, and Ashbolt et al. (1993) isolated S. aureus from primary wastewater, although chlorinated tertiary wastewater had only sporadic occurrences of these organisms. However, there are no publications documenting S. aureus in biosolids. Recent work at the University of Arizona optimized culture media for S. aureus, which was then used to evaluate the presence of the organism in biosolids. Biosolids from Tucson, Arizona, were negative for S. aureus (C.Gerba, University of Arizona, personal communication, June 2002).

Protozoan Pathogens

Cryptosporidium and Giardia are the protozoan parasites most often associated with biosolids. They are parasites of the small intestine that cause diar-

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

rhea. Cryptosporidium oocysts and Giardia cysts have been detected in products of wastewater treatment and anaerobic sewage sludge digestion (Chauret et al. 1999) and in biosolids (Bean and Brabants 2001b). These pathogens have been observed to die within days of Class B biosolids treatment (Bowman et al. 2000). However, there is little research on the survival of these organisms in biosolids-amended soil.

Microsporidia are obligate intracellular parasites (e.g., Encephalitozoon spp.) that have been associated with gastrointestinal illness in patients with acquired immunodeficiency syndrome (AIDS) and in some healthy individuals. One waterborne outbreak has been described (Cotte et al. 1999). Of over 1,200 species described, only 14 have been associated with human infections. At least three of the species that infect humans will grow in animal cell culture (Wolk et al. 2000). No method is available to assess infectivity in environmental samples. The spores of the microsporidia are not unusually resistant to heat (Koudela et al. 1999).

Helminths

EPA considered the human pathogens Ascaris lumbricoides, Trichuris trichiura, Taenia saginata, Taenia solium, Necator americanus, and Hymenolepsis nana in establishing the pathogen standards of the Part 503 rule. Also included were two animal pathogens Ascaris suum (of pigs) and Toxocara canis (of dogs). Human infections with A. lumbricoides, T. trichiura, and H. nana are obtained through direct consumption of embryonated eggs. T. saginata infections in people are typically acquired from the ingestion of beef. The eggs of this organism have been detected in some biosolids (Barbier et al. 1990). The eggs of Taenia solium are infectious to pigs, but also are capable of producing larvae that infect people and can cause central nervous system disease (Bale 2000). People are infected with N. americanus by the larvae penetrating the skin. People who ingest the eggs of A. suum of pigs can develop pneumonic, asthma-like signs and can develop a few single adult worms. People who eat the eggs of T. canis can develop visceral or ocular larva migrans, syndromes that occur mainly in children who eat contaminated dirt (Overgaauw 1997; Taylor 2001).

Recently, concerns have been raised about roundworm Baylisascaris procyonis. The egg of this worm is similar to that of the related Ascaris spp., and the ingestion of the eggs of this parasite can cause severe neurological and ocular disease in humans and has been linked to some fatalities (Sorvillo et al. 2002). However, eggs of B. procyonis have not as yet been identified in biosolids samples.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

TABLE 6–6 Inactivation of Scrapie Prions

Disinfectant

1 5 min (log reduction)

60 min (log reduction)

Hypochlorite (5,250 mg/L)

3

4

Sodium metaperiodate

1.5

3

Iodine

1

2

I2 (20,000 mg/L)

NaI (24,000 mg/L)

 

Phenol (5,000 mg/L)

0.3

1

Hydrogen peroxide

2.5

4

Potassium permanganate

0.3

1

Formaldehyde (200,000 mg/L)

0

1

Lime treatment

-

1

 

Sources: Rohwer 1984; EPA 2001.

Prions

Concern about prions has arisen with the advent of prion animal diseases such as bovine spongiform encephalopathy (BSE) in the United Kingdom and other parts of Europe. The BSE prions concentrate in an animal’s brain and spinal cord, but they have been detected only in sheep blood at low concentrations. Animal manure would have no or low concentrations of BSE prions except possibly for wastes from slaughterhouses (Ward et al. 1984); however, the presence of prions in such wastes is uncertain (EPA 2001). Prions are generally transmitted from animal to animal (cow to cow, sheep to sheep). The risk of prion transmission to biosolids from animals is low but can increase with the presence of small amounts of neural tissues or placenta coming from slaughter houses. At present, there has been little evidence of prion-contaminated manures in the United States.

Prions are very difficult to inactivate and require rigorous treatment (Godfree 2001). The higher the solids content of the waste, the more rigorous the treatment required (EPA 2001). Table 6–6 presents inactivation data for scrapie prions under a variety of disinfection treatments.

Prions are resistant to high temperatures; scrapie prions are inactivated at temperatures of 100°C or above. At 121°C, 0.01% of the prions were resistant to thermal inactivation (Rohwer 1984). Prions have been reported to survive

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

boiling and autoclaving (D.M.Taylor et al. 1999; EPA 2001). Prion survival at increased temperatures coupled with chemical or biological treatment associated with biosolids processing has not been studied, nor are data available to directly assess prion survival through sewage-sludge treatment processes.

In addition to chemical treatment (shown in Table 6–6), gamma radiation is also used to inactivate prions. The required irradiation dose is related to pathogen size. As the size decreases, the gamma dose increases, because it is harder for the gamma irradiation to hit the specific sensitive targets in the smaller infectious agents. The inactivation dose for helminth eggs, viruses, and prions was found to be 200 kilorad (unit of absorbed dose) (McDonell 1985), 1 megarad (Ward et al. 1984), and 5 megarad (Rohwer 1984), respectively.

Rationale for Selecting Emerging Organisms

In the current regulations, the only pathogens considered are enteric viruses, helminths, and Salmonella (or coliforms). In this section, the committee outlines criteria that should be used to identify other pathogens that EPA should review and for which information on occurrence, persistence, and risk should be obtained. Once that information is obtained, a decision can be made on whether biosolids regulations need to be modified to control the risk from these agents or whether the existing regulations suffice to control these agents at an acceptably low level of risk.

The selection of microorganisms for analysis in biosolids or wastewater should based on the following criteria (C.Gerba, University of Arizona, personal communication, September 2001):

  • Reliable viability assay. Availability of a reliable and relatively consistent assay is critical for the study of a pathogen.

  • Water-related disease-causing agents. All selected pathogens must be found in wastewater and should be capable of transmission via exposure (airborne, waterborne, or contact) to biosolids.

  • Extent of existing data on probability of surviving biosolids treatments. The pathogens that have the greatest probability of surviving biosolids treatment processes are increasingly of concern for land application. The pathogens that can survive at high pH (above 11–12) and are heat resistant are of most concern.

  • Extent of survival in the environment. The longer a pathogen survives in the environment, the greater the chance of its transmission to a susceptible host.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

Table 6–7 shows the criteria and a list of the pathogens that can be considered for analysis. On the basis of these criteria, adenovirus 40, astrovirus, hepatitis A virus, rotavirus, and E. coli 0157:H7 are potential target organisms for analysis. In addition, caliciviruses, including Norwalk viruses, are important, but methods of analyzing viability are not currently available. The protozoan parasites were not selected, because they are unlikely to survive the heat treatment, and viability methods are not available for their detection. Although the bacterial pathogens Legionella spp. probably deserve further study, they were not included, because the current detection methods have low efficiency, are difficult to use, and are costly.

Role of Indicator Organisms

The routine examination of biosolids for the presence of human pathogens is often tedious, difficult, and time consuming. Therefore, considerable effort has been made to identify indicator microorganisms whose presence would suggest that human pathogens might also be present. A benefit of using indicator organisms is that tests for them should be simpler and more routine.

In the Part 503 regulation, fecal coliforms are used as indicator organisms in two ways. First, as an indicator of health hazards, fecal coliform density can be used to classify Class A biosolids. Second, as an indicator of wastewater-treatment efficiency, fecal coliform density is used to evaluate whether Salmonella sp. has repopulated when Class A biosolids are stored before land application. Fecal coliforms are an appropriate indicator of treatment efficiency, but because they have the potential for regrowth (Pepper et al. 1993), their use as an indicator for public-health hazards is less justified. In addition, some pathogens are more hardy than fecal coliforms, highlighting the potential for underestimating a specific health hazard.

Clostridium perfringens has been suggested as another possible indicator organism to assess the efficiency of biosolids disinfection processes. C. perfringens, a spore-forming bacteria, is a good monitoring organism for processes using noncharged biocides (molecules that do not carry a net electrical charge, such as NO2 and NH3) or temperatures greater than 120°C (Blanker et al. 1992). It has been suggested as a tracer for less hardy indicators and for the absence of protozoan parasites or viruses during wastewater treatment (Payment and Franco 1993). Because C. perfringens is typically found at densities of 106 colony-forming units (CFUs) per gram of solids in raw or untreated biosolids, its spores might be an excellent surrogate for the eggs of Ascaris suum (Reimers et al. 1991; Sobsey et al. 1991) in the f ollowing systems: oxy-

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

TABLE 6–7 Emerging Pathogens Likely to Be Present in Biosolids

Organism

Reliable Viability Assay

Waterborne Outbreaks

Probability of Surviving Biosolid Treatment

Survival in the Environment

Adenovirus

Yes

Yes

High heat

Low pH

Months

Norwalk virus

No

Yes

Unknown

Unknown

Astrovirus

Yes

Yes

Moderate

Weeks

Hepatitis A

Yes

Yes

High heat

Moderate pH

Months

Rotavirus

Yes

Yes

Moderate

Months

Hepatitis E

No

Yes

Unknown

Unknown

Mycobacterium

Yes

Yes

High

Days

E. coli 0157:H7

Yes

Yes

High

Months, regrowth possible

Legionella

Yes

Yes

Unknown

Yes

Listeria

No

No

High

Weeks

Microsporidia

Yes?

Yes

Low

Unknown

ozone, thermophilic alkaline treatment, two-stage anaerobic digestion, composting, anaerobic digestion, and lagoon storage. C. perfringens spores were selected for monitoring Ascaris egg survival in chemically processed municipal sewage sludge, because both organisms appear to exhibit similar resistance to physical and chemical agents (heat, alkaline pH, hydroxide concentration, and nitrous acid content). The external structures of both microorganisms may account for some similarities in resistance and inactivation; however, the Ascaris egg is more sensitive to high temperatures (>45°C) (Blanker et al. 1992), whereas C. perfringens spores, unlike other indicator microbes, are not inactivated in thermophilic processed sewage sludge. Furthermore, C. perfringens is susceptible to hydroxide, whereas Ascaris eggs are resistant to high concentrations. Ascaris is very sensitive to high concentrations of ammonia (0.05% to 2%), depending on temperature (Blanker et al. 1992). Detection of airborne clostridia is dependent on a method for analyzing biosolids-generated bioaerosols (Pillai et al. 1996; Dowd et al. 1997). Unlike most microbial bioaerosols, spore-forming bacteria are resistant to desiccation.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

Other anaerobic bacteria, such as Bifidobacterium and Bacteroides, have also been suggested as potential indicators. However, better standard methods for detecting anaerobic bacteria are needed before they can be routinely monitored.

Bacteriophages have also been suggested as indicators of fecal matter and viruses, because they are consistently found in sewage. Somatic coliphage infects E. coli strains and can be detected by simple and inexpensive techniques within 18 h.

A concern with the parasite criteria in the Part 503 regulations is the lack of a timely method to monitor indirectly for the inactivation of Ascaris eggs. Ascaris inactivation is used to determine whether a disinfection process produces Class A biosolids. The direct method of studying Ascaris egg inactivation requires recovering the eggs from biosolids and placing them in culture for 3 to 4 weeks and then examining the culture microscopically. This method is costly, and few laboratories accurately perform the assay. A reliable indirect method requiring only a few days would be beneficial, as would inexpensive, simple, and viable techniques to monitor helminth eggs by surrogate microbes. C. perfringens could possibly be a good indicator organism for Ascaris inactivation where noncharged chemical species are utilized as disinfection agents (e.g., ammonia). However, when temperature is the controlling inactivating factor, a different type of indicator organism or monitoring of temperature and time directly would be needed.

EXPOSURE TO PATHOGENS

The major routes of potential human exposure to pathogens in biosolids are air, soil, water, and vectors. Factors that affect exposure by each of these routes are discussed below.

Air

Land application of biosolids may result in the formation of infectious bioaerosols. Bioaerosols are defined as aerosolized biological particles, ranging in diameter from 0.02 to 100 micrometers (μm) (Dowd and Maier 2000). The composition, size, and concentration of the microbial bioaerosols vary with the source, dispersal mechanisms, and, most important, the environmental conditions at a particular site. Bioaerosols generated from water sources during splashing and wave action often consist of aggregates of several micro-

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

organisms (Wickman 1994) and usually have a thin layer of moisture surrounding them. Bioaerosols released into the air from soil surfaces, such as those surrounding biosolids and composting facilities, are often single organisms or are associated with particles. In many instances, these particles serve as “rafts” for microorganisms (Lighthart and Stetzenbach 1994).

The dispersal and settling of bioaerosols is affected by their physical properties and the environment in which they are airborne. The most important physical characteristics are the size, density, and shape of the droplets or particles, and the most important environmental characteristics are air currents, relative humidity, and temperature (Lighthart and Mohr 1987; Pedgley 1991). Nonspecific open-air factors have also been reported to play a role (Cox 1987).

Aerosols can originate from point (e.g., a biosolids pile) or area (e.g., an agricultural field spread with biosolids) sources (Dowd et al. 2000). Point sources can be further categorized into instantaneous (e.g., sneezes) or continuous sources (e.g., release of bioaerosols from a biosolids pile). The launch patterns of bioaerosols from point sources have a conical dispersion pattern, whereas bioaerosols from area sources have a particulate-wave type of dispersion. Bioaerosol transport can be defined in terms of distance and time, submicroscale transport being less than 10 min and distance less than 100 meters (m), as is common in indoor environments. Microscale transport ranges from 10 min to 1 h and from 100 m to 1 kilometer (km). Mesoscale and macroscale transport are greater than 1 h (Hugh-Jones and Wright 1970). Atmospheric turbulence influences the diffusion and thus the concentration of bioaerosols. Bioaerosol stability varies among bacteria, viruses, and other microorganisms.

Although there are reports on pathogen occurrence and survival on agricultural lands and waterways exposed to biosolids, there is surprisingly little information on airborne pathogen occurrence during land application of biosolids. Most aerosol studies have been conducted near water treatment plants, at effluent spray irrigation sites, within waste-handling facilities, and at composting facilities (Lembke et al. 1981; Brenner et al. 1988; Millner et al. 1994). Different bioaerosol-sampling methods can lead to recoveries of different organisms. Sorber et al. (1984) used a large volume electrostatic precipitator air sampler to study bioaerosols from the land application of biosolids. They showed that bioaerosols are generated during the application of biosolids by tanker trucks and at spray irrigation sites. However, enteric viruses were not detected in the bioaerosol samples that were analyzed. In studies conducted at a large land-application site in Texas, Pillai et al. (1996) used an AGI-30 impingement-based sampler to detect bioaerosolized micro-

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

bial populations, including bacteriophages. Under low-wind conditions, none of the samples contained any presumptive Salmonella spp., although some of the samples were positive for hydrogen sulfide-producing organisms and pathogenic clostridia. In subsequent monitoring during high-wind conditions, fecally associated male-specific coliphages, thermotolerant clostridia, and presumptive Salmonella spp. were also detected (Dowd et al.1997). Bioaerosol concentrations were higher at sites where biosolids material was physically agitated as compared with sites where “manure applicators” were used. These studies were used to generate microbial release rates from biosolids to model bioaerosol transport (Dowd et al. 2000) and, in conjunction with assumed dose-response relationships, to compute an estimated risk.

Exposed people might develop allergic and toxic reactions to high concentrations of noninfectious microorganisms. The health effects from exposure to such agents have been well documented in sewage treatment plants, animal housing facilities, and biowaste collection sites. Studies using culture-based and nonculture-based methods have indicated that workers at the sites can be exposed to concentrations of microorganisms as high as 102–109 CFU/m3 and 104–1010 microorganisms per cubic meter, respectively. Such exposures are substantially higher than those generally found indoors (Eduard and Heederik 1998).

Several studies have documented that microbial bioaerosols are strongly linked to waste-application practices, biosolids handling, wind patterns, and micrometeorological fluctuations (Brenner et al. 1988; Lighthart and Schaffer 1995; Pillai et al. 1996; Dowd et al. 1997). Studies conducted on land-applied Class B biosolids have shown that physical agitation of biosolids material releases Salmonella and fecal indicator viruses (Dowd et al. 1997). Bioaerosols averaging 300 most probable number of presumptive Salmonella spp. per cubic meter were detected at biosolids loading and application sites at an arid location in the United States. The detection of microbial pathogens at distances from the point source is indicative of how wind gusts and wind patterns can transport bioaerosols over distances.

Mathematical models have been designed to predict the transport of microorganism-associated bioaerosols. Pasquill (1962) described a classic model of particulate airborne transport of aerosols launched from a continual point source. Lighthart and Frisch (1976) modified Pasquill’s equation to include a microbial inactivation constant to account for ultraviolet radiation inactivation and desiccation during transport. Bioaerosol sampling used in conjunction with aerosol transport models can be used to estimate inhalation exposure. These estimates in turn can be used in microorganism-specific dose-response models to determine the risks of infection (Haas et al. 1999a).

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

On the basis of field-sampling data, Dowd et al. (2000) modeled microorganism concentrations based on point and area sources at a biosolids application site in the arid western United States at distances ranging from 100 to 10,000 m and windspeeds ranging from 1 to 20 m/s (4.5 m/s is the average U.S. windspeed). As expected, the projected risk of infection from exposure to a single organism was greater at higher windspeeds and closer to the source and was correlated with duration of exposure. The risk of infection at 1,000 m was predicted to be low; however, at 100 m, the potential risks of bacterial and viral infections ranged between 1% and 29% (between 1/100 and 29/100). It is important to note that this is a worst-case situation based on the method of application, which tossed biosolids into the air. Application was done in this manner because there were no towns or human populations in close proximity to the land-application site.

Soil

Pathogen survival in and transport through soil are considered together in this section. Environmental factors that affect survival of pathogens are summarized in Table 6–8. Human pathogens that are routinely found in domestic sewage sludge include viruses, bacteria, protozoan parasites, and helminths. Of those pathogens, viruses are the smallest and least complex, generally have a short survival in soil, and have the greatest potential for transport in soil. Using a plaque-forming-unit method, Straub et al. (1993a) evaluated the survival of three viruses in a biosolids-amended desert soil: poliovirus type 1 and two bacteriophages (MS2 and PRD-1). Survival was temperature-dependent and decreased as temperature increased. Soil type affected virus survival, longer survival occurring on clay loam biosolids-amended soils compared with sandy loam biosolids-amended soils (Straub et al. 1993b). Rapid loss of soil moisture also limited virus survival. When conventional plaque-forming methods were used, virus survival ranged from 3 days to greater than 10 days, depending on soil type, temperature, and moisture (Straub et al. 1992, 1993a). When molecular polymerase chain reaction (PCR)-based methods were used, enteroviruses were detected in soil 3 months after land application (Straub et al. 1995). However, PCR by itself only detects viral nucleic acid and does not indicate that viable viruses were actually present.

Like virus survival, bacteria survival in soil is affected by temperature, pH, and moisture (Gerba et al. 1975). Soil nutrient availability also plays a role in bacteria survival. Lower temperatures usually increase survival, as do a neutral soil pH and soil at field capacity (Straub et al. 1993b). Of the pathogenic bacteria, Salmonella and E. coli (Newby et al. 2000b) can survive for a long time

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

TABLE 6–8 Environmental Factors Affecting the Survival of Pathogenic Microbes

 

Survival Time

Parameter

Virus

Bacteria

Protozoa

Temperature increasing

Soil moisture decreasing

Rate of desiccation increasing

Clay content increasing

+

+

Not known

pH range of 6–8

+

+

0

Note: −, decreasing survival time; +, increasing survival time.

Sources: Gerba et al. 1975; Straub et al. 1993a,b, 1995; Jenkins et al. 1999.

in biosolids-amended soil—up to 16 months for Salmonella (Hess and Breer 1975). In contrast, Shigella has a shorter survival time than either Salmonella or E. coli (Feachem et al. 1983). Studies on indicator organisms have shown that total and fecal coliforms as well as fecal streptococci can survive for weeks to several months, depending on soil moisture and temperature conditions (Pepper et al. 1993).

Regrowth is also important when evaluating the survival of pathogenic and indicator bacteria in soil and biosolids compost. Salmonella, E. coli, and fecal coliforms are all capable of regrowth. Following land application of biosolids or composting of biosolids with soil, pathogen concentrations decrease below the detection limit but subsequently increase after rainfall (Pepper et al. 1993; Soares et al. 1995; Gibbs et al. 1997).

The protozoan parasites often associated with biosolids include Giardia and Cryptosporidium spp. However, little research has been conducted on the survival of these parasites in biosolids-amended soil. One report documented increased inactivation of Cryptosporidium parvum as temperature increased from 35°C to 50°C and water potential decreased (Jenkins et al. 1999). Little is known about the viability of these parasites following land application of biosolids, and research in this area should be encouraged. Helminths are perhaps the most persistent of enteric pathogens. Ascaris eggs survive several years in soils, although very dry or very wet soils decrease survival (Straub et al. 1993b).

The transport of microorganisms through soils or vadose zone materials is affected by a complex array of abiotic and biotic factors, including adhesion processes, filtration effects, physiological state of the cells, soil characteristics,

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

water flow rates, predation, and intrinsic mobility of the cells (Newby et al. 2000a), as well as the presence of biosolids. For viruses, the potential for transport is large, although viruses can adsorb to soil colloidal particles and to the biosolids themselves, thus limiting transport (Schijven and Rietveld 1996). Virus sorption is controlled by the soil pH. Most viruses are negatively charged (isoelectric point 3–6) so that at a neutral soil pH, soil sorption is reduced, whereas at more acidic soil pH values, the viruses are positively charged, increasing sorption. Dowd et al. (1998) confirmed that the isoelectric point was the predominant factor controlling viral transport through soil; however, for virus particles greater than 60 nanometers (nm) in diameter, size began to limit transport. The sorption of bacteriophages and viruses to nine soil types was examined by Goyal and Gerba (1979), who confirmed that sorption is greatest at soil pH values of less than 5.

There are few field studies on the transport of viruses from biosolids through soil. Most studies on virus transport have been conducted in laboratory columns, using pure virus cultures. Straub et al. (1995) evaluated transport of enteroviruses from land-applied, anaerobically digested biosolids. Viruses were detected at soil depths of 200 centimeters (cm), indicating greater transport than that reported in previous studies (Damgaard-Larsen et al. 1977; Bitton et al. 1984). In the Straub study, a more modern PCR-based detection method was used, rather than the conventional cell-culture methods used in earlier studies. However, PCR alone does not indicate viability of the viruses.

The larger size of bacteria means that soil acts as a filter, limiting bacterial transport. Soil would also limit the transport of the even larger protozoa and helminths (Newby et al. 2000a). However, microorganisms may be transported through soil cracks and macrochannels via preferential flow. Transport of indicator organisms from land-applied, anaerobically digested biosolids was evaluated by Pepper et al. (1993), who found occasional fecal coliforms at soil depths of 300 cm, presumably due to preferential flow.

Pathogen survival and transport in soil should be evaluated from a public-health perspective. Pathogens are routinely present in Class B biosolids and are capable of surviving for days, weeks, or even months, depending on the organism and environment. Therefore, site restrictions with durations based on subsequent land use are necessary following land application. For many soils, contamination of underground aquifers due to vertical migration of pathogens from land-applied biosolids is unlikely because of the sorption of viruses and the soil filtration potential for larger pathogens. However, in coarse textured, sandy soil or high permeability karst topography, groundwater contamination events are possible. For example, surface-water contamination can occur from land-applied biosolids because of soil runoff. In the U.S., groundwater sources unrelated to biosolids have been associated with 58% of

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

total waterborne-disease outbreaks, compared with 33% from surface-water sources (Schijven 2001). The committee notes that there is a dearth of contemporary information on pathogen transport through and on soil from land-applied biosolids in field situations. The transport of pathogens through biosolids-amended soil is different than from soil alone because of sorption and binding to the biosolids.

Water

In principle, pathogens present in biosolids can contaminate surface or groundwaters if runoff and leachate are not controlled. When municipal solid waste is landfilled, microbial contamination of groundwater from leachate is possible, albeit at low levels (Sobsey et al., 1975; Sobsey, 1978; Pahren, 1987). Ritter et al. (1992) found that lime-treated septage applied to land did not deteriorate groundwater quality in regard to pathogens. The committee did not identify any studies of microbial contamination of surface or groundwater near land where either Class A or Class B biosolids had been applied.

Vectors

There are no published reports that specifically implicate vectors in the transmission of infectious organisms from land-applied biosolids to humans. However, there have been reports of fly proliferation and mosquitos in standing water bodies, such as sewage effluent and septic tanks (Carlson and Knight 1987; D.S.Taylor et al. 1999; Learner 2000). A number of studies indicate that vectors such as flies, rodents, and birds harbor infectious agents commonly associated with animal and poultry wastes. Butterfield et al. (1983) reported that herring gulls carry Salmonella, and Juris et al. (1995) reported that flies disseminate helminth eggs from sewage treatment plants. Although data (Grubel et al. 1997) suggest that houseflies harbor Helicobacter pylori, direct transmission of the organism from flies to humans has not been demonstrated. Although flying insects are usually attracted to odors (Morris et al. 1997), there are no published data on whether land application of biosolids results in an increase in flies, mosquitoes, or birds. If biosolids application is not managed properly, heavy rainfall in conjunction with biosolids application could result in pools of biosolids-contaminated runoff that could attract vectors. Land-application practices as specified in the Part 503 rule are designed to reduce vector attraction, but it is unclear whether these practices discourage vectors. Although flies and other vectors have been detected on biosolids-

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

applied lands, the extent to which these vectors are involved in the transmission of infectious organisms to humans or the food chain is unknown.

Regional Differences

The extent and routes of human exposure to biosolids vary greatly across the United States, depending on the overall “experience with biosolids use.” Four exposure factors that vary by region are methods of biosolids application, climate, soils, and land availability for biosolids application versus population density.

  • Methods of Biosolids Application. Biosolids-application methods vary depending on region, type of biosolids, and individual site. For example, in the southwestern desert, liquid anaerobic-digested biosolids are generally injected into soil subsurface. On pastures, biosolids are generally applied to the soil surface. In other areas, biosolids “cakes” are added and disked into soil. The application method directly affects the potential for bioaerosol generation, chemical odors, and ultraviolet inactivation of pathogens. It is important to note that incorporation of biosolids is more difficult with pastureland than cropland.

  • Climate. Regional differences in climate affect the fate and transport of pathogens in biosolids-amended soil. In general, moist, cool soils, such as those in the northeastern region of the United States, favor survival, whereas hot, dry soils, such as those in the southwestern region, adversely affect pathogens. Differences in rainfall are not as important as temperature, because application of biosolids on desert agricultural lands is often followed by irrigation.

  • Soils. Although climate affects regional soil types, texturally, all soil types can be found throughout the United States. Of all soil characteristics, soil pH differences are perhaps the most important. Typically, more acidic pH ranges and more organic matter are in soils east of the Mississippi than in the more arid western states.

  • Land Availability and Population Density. Land availability and population densityare the most important factors for acceptability of the “experience with biosolids use.” In the desert Southwest, agricultural areas are often located far from urban centers, so that there are fewer surrounding residents who may be affected by biosolids applications. In the Northeast, the potential impact of land application is much greater because of the magnitude of land application and the proximity of that land to people. For example, in areas such as Rhode Island, almost all land would need to receive biosolids to

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

accommodate use and disposal. In high-density urban centers, there is an increased potential for nuisance odors and for increased exposure to pathogens. Thus, the regional differences in land availability for biosolids application relative to the proximity of urban centers mean that “experience with biosolids use” is not uniform nationwide.

HOST FACTORS

Assessing potential risks from exposure to pathogens is complicated by the need to consider a variety of factors that affect an individual’s susceptibility to pathogens. Three of these factors, concomitant exposures, genetic factors, and acquired immunity, are discussed below.

Concomitant Exposures

Studies have shown that concomitant exposures to infectious organisms, noninfectious organisms, cellular components, irritants, and odors can cause synergistic effects, especially in humans in highly contaminated environments (Schiffman et al. 2000). For example, the adverse health effects from exposure to a combination of ammonia and particles were greater than the additive effects of ammonia and particles by a factor of 1.5 to 2.0 (Bottcher 1998, as cited in Schiffman et al. 2000).

Particles, allergenic constituents, and microbial metabolites, such as endotoxins (lipopolysaccharides [LPS]), glucans, and aflatoxins, can have a role in the development of various respiratory diseases and systemic effects (Eduard and Heederick 1998). Chromogenic end point and kinetic endotoxin assays are used to estimate the relative biological activity of LPS rather than measure the exact amount of LPS present. However, there are accuracy and reproducibility concerns with these assays (Hollander et al. 1993). Carbohydrate components of molds, such as glucans and mannans, are known to act as inflammatory agents and can function as biomarkers for exposure to molds (Murphy 1990).

Because endotoxins and glucans are cellular components of microorganisms, anaerobic digestion would not be expected to totally destroy or inactivate those compounds. The detection of viable cells in land-applied biosolids implies that endotoxins should also be present. However, local climatic and biosolids-management practices dictate the extent of endotoxin aerosolization. Van Tongeren et al. (1997) reported considerable variation in endotoxin concentrations in municipal wastes at a compost plant, with concentrations rang-

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

ing from 0.2 ng/m3 at a compost plant to 353.6 ng/m3 at a waste-resource recovery operation. Nielsen et al. (2000) found seasonal variations in endotoxin concentrations around operations involving containers of biosolids; concentrations ranged from 0.3 ng/m3 in spring to a maximum of 100 ng/m3 in autumn. Ivens et al. (1999) reported a direct relationship between bioaerosol concentrations of endotoxins and nausea and diarrhea among waste collectors. Endotoxin concentrations ranged from 0.36 enzyme unit (EU)/m3 to 9.2 EU/m3 (0.03 ng/m3 to 0.77 ng/m3, assuming 1 EU=12 ng/m3). Melbostad et al. (1994) reported that municipal sewage workers in Norway were exposed to endotoxin concentrations of 0–370 ng/m3 over 8 h (median level, 30 ng/m3); however, no relationship was seen between endotoxin concentrations and such symptoms as nausea, tiredness, and headaches.

People with atopic asthma have increased sensitivity to respirable endotoxins, resulting in a variety of immune responses, including increased eosinophils in the airways (Peden et al. 1999). Studies suggest that asthmatic individuals exposed to allergens will have greater nasal inflammations if exposed to endotoxins (Gavett and Koren 2001; Liu and Redmon 2001; Reed and Milton 2001).

Genetic Factors

Data suggest that host genetic factors (e.g., predisposition to asthma attacks) have a key role in the manifestation of a health effect from infectious organisms, particles, odors, endotoxins, or allergens (Lacey and Crook 1988; Michel et al. 1991, 1992, 1996; George et al. 2001). These studies have been conducted on biowaste collectors, compost workers, sewage treatment plant workers, and animal house workers, who are constantly exposed to high concentrations of these agents. There are no data on the roles of genetic factors in health effects due to bioaerosols from land-applied biosolids. Furthermore, although particles, allergens, and microorganisms can cause health effects in occupationally exposed workers, data are lacking on whether the concentrations observed at land-application sites are sufficient to cause health effects in surrounding populations.

Acquired Immunity

A potential factor modulating the risk from exposure to infectious agents is acquired immunity, which can reduce the extent of illness in a population exposed to microbial contamination or alter the dynamics of disease occur-

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

rence. For most agents of concern, the existence, extent, and duration of any acquired immunity is not well understood. For a number of infections, immunity may be highly short-lived (Anderson and May 1991; Bailey 1975). In the case of Salmonella, only partial immunity appears to occur, resulting in reduced severity (McCullough and Eisele 1951). In the case of Cryptosporidium, there is also some reduction in susceptibility following an infection, although in some cases the severity of the infection in individuals rechallenged may be more severe (Chappel et al. 1999).

If information on the extent and duration of immunity is found, it can be incorporated into population models of infectious disease, as described in Chapter 7.

EXPOSURE TO WORKERS

Sewage sludge and biosolids are used in a number of ways, including application to agricultural fields, recreational fields, lawns, and home gardens and reclamation of mines and other disturbed lands. The process of preparing and applying biosolids involves workers who are potentially at risk of exposure to infectious pathogens in the sewage sludge during preparation in the treatment plant, transportation of the biosolids to places of application, application to land, and following application in the fields. The worker populations were not considered in setting EPA’s standard for pathogens in biosolids. As reported in Chapter 3, there are few studies of worker exposure to biosolids. However, there are a few studies of exposure and effects observed in workers at wastewater and sewage treatment plants. Although these studies are not substitutes for studies of biosolids exposure, they are useful for identifying potential health concerns and pathogens that might be relevant to biosolids.

The presence of human pathogens in raw sewage sludge has been well documented. Ayres et al. (1993) reported on the accumulation and viability of human nematode eggs (primarily Ascaris lumbricoides) in the sewage sludge of a waste-stabilization pond. Cryptosporidium oocysts and Giardia cysts were recovered from products of wastewater treatment and anaerobic sewage sludge digestion (Chauret et al. 1999). Specific infectious agents have been recovered from biosolids applied to land, including eggs of the helminth Taenia saginata (Barbier et al. 1990). Thermotolerant clostridia were detected in aerosols from a large commercial application site (Dowd et al. 1997). In a multiyear study, 21 Salmonella serotypes were isolated from sewage sludge from four treatment plants in different geographic areas of Ohio (Ottolenghi and Hamparian 1987). In the same study, family members residing on farms showed antibodies to salmonellae, but the investigators were unable to deter-

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

mine whether there was a significant difference between exposed and control subjects.

Immunoglobulin G antibodies to molds and actinomycetes were found in biowaste collectors and compost workers exposed to bioaerosols (Bünger et al. 2000). Higher exposures to rod-shaped and total bacteria were found in sewage workers with airway symptoms, headache, tiredness, and nausea than in workers not reporting these symptoms (Melbostad et al. 1994). Hepatitis A was reported in workers from a wastewater treatment plant during a small community outbreak (De Serres and Laliberté 1997).

ANTIBIOTIC RESISTANCE

There is constant acquisition and loss of genetic sequences among bacteria (Ochman et al. 2000). Bacteria can acquire antibiotic resistance through point mutations, plasmid transfer events, transposons, and integrons. Mobile DNA sequences make up a substantial portion of the transferred sequences in E. coli (Lawrence and Ochman 1998). There are reports that antibiotic-resistant organisms can be isolated from biosolids (Pillai et al. 1996, 1997), and antibiotic resistance transfer events have been documented under laboratory conditions in sewage effluent (Arana et al. 2001). A recent study found tetracycline-resistance genes in waste lagoons and groundwater at two swine production facilities (Chee-Sanford et al. 2001). This study also suggested that the resistance genes can be mobilized into soil inhabitants. However, there are no data to suggest that land application of biosolids will preferentially promote such transfer events. Assuming that biosolids contain a number of potential donors and recipients of antibiotic resistance genes, it is important to keep in mind that multiple processes should occur for the stable incorporation and expression of new traits in the recipient cells. The donor DNA must be delivered to the recipient cells, the transferred genes should be incorporated into the recipient’s genome or plasmid, and finally, the incorporated genes should be expressed in a manner that benefits the recipient cells (Ochman et al. 2000). A German study suggests that there is minimal likelihood of functional antibiotic compounds persisting in biosolids (Hirsch et al. 1999); therefore, it is doubtful whether the incorporation and maintenance of antibiotic resistance genes in recipient cells would provide them with any selective advantage. Antibiotics are, however, present in raw sewage sludge and sewage treatment plant effluent. Resistant bacteria can therefore be present in biosolids without a selective advantage in that medium and without specific gene transfer in that medium. Pillai et al. (1997) reported no significant differences in the antibiotic resistance index of E. coli isolates obtained from undigested and digested

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

municipal sewage from rural and urban environments when 13 antibiotics were screened. The ability of biosolids-related organisms to transfer their resistance markers to indigenous soil bacteria would depend on the survival of the introduced strains in addition to the factors mentioned above. On the basis of this information, the committee does not believe that land-applied biosolids have any substantial potential to alter the prevalence of antibiotic resistance among pathogenic microorganisms.

PATHOGEN RISK ASSESSMENT

Risk assessment has been used in several environmental and public-health applications to determine (or reduce) exposure to pathogenic microorganisms. In this section, available approaches to conducting microbial risk assessment are briefly reviewed and their applicability to biosolids is assessed. The committee was aware that methodology for assessing risks to human health from pathogens via exposure to biosolids is being developed by researchers at the University of California at Berkeley. The methodology has an exposure-assessment component for quantifying pathogen levels and a health-risk component that accounts for special infectious disease considerations (secondary transmission and immunity) (J.Eisenberg, University of California, Berkeley, personal communication, May 24, 2002). However, the methodology was not finalized in time for the committee to evaluate it and include it in this report.

Drinking Water

Historically, the acceptable levels of microorganisms in drinking water, contact recreational waters, and shellfish harvesting waters have been set using indicator organisms, most often either total or fecal coliforms. With the advent of better methods for direct measurement of pathogens in water (Leong 1983; Ongerth 1989; Gerba and Rose 1990; Gregory 1994; Rose 1990; Rose et al. 1991a) and the development of risk-assessment paradigms for setting environmental standards (NRC 1983, 1989; Silbergeld 1993), these methods can now be applied to the development of microbial standards for acceptable water quality to supplement or replace traditional indicator measurements.

The quantitative microbiological risk assessment (QMRA) approach that has been used in the development of the Surface Water Treatment Rule (SWTR) and the Enhanced SWTR follows the framework proposed for chemical risk assessment by the National Research Council (NRC 1983). The framework has the same steps as those for chemical risk assessment: hazard

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

assessment, exposure assessment, dose-response analysis, risk characterization, and risk management.

Alternative protocols specific to microbial risk assessment have been proposed by such groups as the International Life Sciences Institute (ILSI) Pathogen Risk Assessment Working Group (1996). A schematic of the ILSI protocol is shown in Figure 6–2. This protocol emphasizes the interrelationships between the technical and policy-making components surrounding the risk-assessment process, particularly at the problem-formulation stage.

A quantitative microbial risk-assessment approach has, in part, been used by EPA. Using data from human volunteer studies, Regli et al. (1991) developed a dose-response relationship for infection from the ingestion of Giardia lamblia. The result was compared with infection rates observed from waterborne outbreaks to assess the likelihood that an infected person would become ill (Regli et al. 1991; Rose et al. 1991b). Using a target risk of one infection per 10,000 persons per year, which was regarded as acceptable by EPA in the SWTR and a daily average water consumption of 2 liters (L) per person per day, EPA estimated that an acceptable finished water concentration would be 6.75×10−6 organism per L (one organism in 148,000 L). Verification of such low microbial occurrence represents a technological impossibility; therefore, it is necessary to use an estimated finished water concentration based on the microbial quality of source water and the reduction of microorganisms achieved by a particular set of treatment processes.

In the proposed SWTR, a tiered treatment requirement incorporated this approach; however, the final promulgated regulation required a single fixed-value reduction (in logs), which was based on an estimated upper value of source-water microbial concentrations across the United States.

Under the Long-Term Enhanced Surface Water Treatment Rule (LT2ESWTR), surface-water treatment plants will be required to use control strategies based on the concentrations of Cryptosporidium oocysts found in their source water. Although not explicitly founded on risk assessment, the relationship between the oocyst concentrations in source water and the required degree of control is predicated on achieving a minimal degree of public-health protection, regardless of source-water quality.

Food and Air

The methods for assessing risks from exposure to pathogens in food and air are still in their infancy. Several modeling approaches have been used, but modeling pathogens pose specific challenges, such as how to model dose-response relationships (Coleman and Marks 1998) and pathogen reduction or

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

FIGURE 6–2 Schematic of ILSI microbial risk analysis protocol. Source: Adapted from ILSI Risk Science Institute Pathogen Risk Assessment Working Group 1996.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

multiplication in food. There are also the issues of susceptibility, particularly for sensitive subpopulations, such as children, the elderly, pregnant women, and immunocompromised individuals (Balbus et al. 2000), and the potential for secondary transmission of disease.

A general framework for microbial food-safety risk assessment has been proposed by McNab (1998), but this framework requires refinement of appropriate distributions and mathematical relationships before it can be applied to a specific pathogen. In the past 10 years, the U.S. Department of Agriculture has developed risk-assessment models for pathogens in foods of animal origin, focusing on Salmonella in eggs (FSIS 1998a) and E. coli in beef (FSIS 1998b). Another study (Marks et al. 1998) used E. coli 0157:H7 to demonstrate dynamic-flow tree modeling. In an assessment of bioaerosol transport and biosolids placement and the risk of bacterial and viral pathogens, both point-and area-source risk-assessment modeling approaches were used (Dowd et al. 2000).

Applicability of Available Approaches to Biosolids Standards

Methods for conducting microbial risk assessment have advanced substantially since the promulgation of the Part 503 rule. Although these methods have not progressed as far as those for chemical risk assessment, the committee believes that they can be used by EPA as a basis to develop criteria for biosolids to maintain acceptable levels of risk from microbial exposure.

The committee envisions an approach conceptually similar to that used in developing the SWTR and LT2ESWTR. From stipulation by EPA of an acceptable risk level for a particular pathogen, the concentrations in biosolids, either at the time of disposal (where there is immediate potential for exposure) or after a required holding period, can be computed by application of QMRA methods. EPA can then develop experimentally based relationships between process conditions (e.g., time, temperature, pH, chemical doses, and holding times) and indicator organism concentrations (either density or reduction through treatment) that can ensure consistent attainment of the target maximum acceptable pathogen concentrations. A regulation can then be crafted to mandate achievement of particular process conditions and indicator densities or reductions to produce acceptable biosolids for the designated use.

The committee does not recommend that QMRA methods be required by regulation to monitor potential risks at any particular site. Such monitoring should be conducted by using indicator organisms and controlling operational parameters and practices, such as temperature, time, buffer zones, and pH, so that tolerable risk levels are not exceeded.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

To conduct microbial risk assessments, a variety of information is needed, including concentrations of the pathogen in biosolids, its fate and transport in environmental media, and its infectivity (dose-response relationship). The extent of the available data on specific pathogens varies, and there are a number of difficulties with obtaining the needed information and conducting the risk assessments. Some of the obstacles include limitations with available sampling and detection methods, lack of dose-response data, inadequate information on infectivity from inhalation and dermal routes of exposure, and difficulties with population-level modeling. These obstacles are discussed in more detail below.

Potential Limitations in Sampling and Detection Methods
Bacteria

Better sampling and detection methods are needed for pathogens in bioaerosols. Impaction, impingement, filtration, and electrostatic precipitation are some of the methods routinely used to concentrate microorganisms from bioaerosols. There are important differences in the equipment and collection efficiencies of these methods. The ASTM (2001) standard (E-884–82) for assessing occupational exposures to bioaerosols in indoor facilities uses an impinger (AGI-30) to sample a total volume of 240 L of air in 20 min. Currently, there is no standard for assessing occupational exposures from bioaerosols in outdoor environments, such as biosolids-application sites. Although specific microbial pathogens and fecal indicator organisms from biosolids-application sites have been detected using the AGI-30 sampler, there are studies showing that the AGI-30 is relatively inefficient at concentrating bacterial cells from bioaerosols. Samplers with improved airflow rates (up to 400 L/min), concentration efficiency, and portability have been developed to detect bioaerosols, primarily for biological weapons research, and are commercially available. Although many of these samplers have been reportedly field tested for their efficacy in detecting biological weapons, peer-reviewed published data on their efficacy are not available. The limitations of commercially available bioaerosol samplers include considerable variation in sampling efficacy (Juozaitis et al. 1994), ability to culture some microbial samples, and ability to characterize the microbial populations beyond plate counts. During transport, deposition, and sampling, bacteria can be inactivated or desiccated. The “injured” cells might be incapable of being cultured on routine microbiological media, thus underestimating the actual number of viable cells within a bioaerosol. For example, the Anderson sampler, which relies on an impac-

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

tion-based sampling approach, has provided a large amount of data on indoor bioaerosols. Because the Anderson sampler is based on impaction and the microbial population estimates are based on direct plate counts, the impaction-based sampling approach can lead to an underestimation of the actual bioaerosol load for the following reasons. First, bioaerosolized organisms may be in a viable but non-culturable state, thereby not forming colonies on the plates. Second, the larger cut-off size of the sixth stage of the Anderson sampler may make it inefficient at collecting very small bioaerosolized particles (Terzieva et al. 1996). A key limitation in bioaerosol sampling is the portability of the samplers for use in remote field sites. Many of the samplers, such as the AGI-30, that rely on external vacuum and power sources cannot be easily used at remote sites. The hand-held, highly portable SAS surface impaction-based sampler has been used for monitoring; however, the samples are impacted on a solid surface, which can be extremely detrimental to their survival and culture.

Some molecular-biology-based assays, such as gene-probe hybridization and gene amplifications, have promise for detecting and characterizing specific microbial groups within bioaerosols. However, those methods have some technical shortcomings, such as inhibitory sample effects, sample processing deficiencies, laborious protocols, and possible laboratory-based contamination (Alvarez et al. 1995, Pena et al. 1999). Droffner and Brinton (1995) have detected Salmonella-specific nucleic acids within thermophilic compost piles, suggesting that microbial nucleic acids can be resistant to degradation, even at the raised temperatures found in compost piles. However, the detection of stable nucleic acid sequences does not imply the presence of viable organisms; therefore, molecular analyses, such as gene probe hybridizations and gene amplifications, should be interpreted with caution. Furthermore, because noninfectious microorganisms and microbial components (e.g., cells, spores, endotoxins, glucans, chemical markers, antigens, and allergens) might cause allergic and toxic reactions independent of cell viability, nonviability-based assays are also necessary (Eduard 1996).

Another concern in assessing the potential impacts of pathogen-laden bioaerosols from biosolids-application sites is the sampling scheme. Land-application programs may involve tens of acres with highly variable micrometeorological conditions within the same general site. The fluctuations can be due to topography, vegetation, and mechanical agitation. Wind direction and speed also can fluctuate, even within a 20-min sampling time. Because no standards exist for bioaerosol sampling in outdoor environments, the exact number of replicate samples needed to get a fair representation is unclear. The choice of an appropriate statistical analysis to give environmentally significant conclusions is also important. Spicer and Gangloff (2000) reported

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

on the limitations of using data on nonparametric statistical treatments of bioaerosols. A further concern is that the definition of upwind and downwind sampling locations at sites may be too broad for bioaerosol samplers with sampling orifices of only a few centimeters in diameter.

Thus, there are challenges to developing and implementing an effective bioaerosol-monitoring program, including the need for a rigorous sampling scheme, integrated sampling to account for micrometeorological fluctuations (which may be the most important challenge from a public-health standpoint), and the lack of efficient and portable bioaerosol samplers. Other than the ASTM standard sampling protocol for evaluating the microbiological quality of municipal solid wastes (ASTM 2001) there are no standardized sampling schemes for determining the bacteriological and viral quality for biosolids land-application programs. Standards are needed for bioaerosol sampling that account for outdoor site characteristics, especially variations in site size.

The environmental conditions under which microbial pathogens are aerosolized from biosolids piles at field sites and from biosolids applied to agricultural land need to be accurately determined. The precise composition of biosolids material and bioaerosols from those sites also need to be studied using conventional and contemporary molecular tools, such as qualitative and quantitative PCR assays, and the bacterial isolates archived. Archived isolates permit the use of DNA fingerprinting methods to determine whether the isolates originate from land-applied biosolids (Dowd and Pillai 1999).

Viruses

Sewage sludge and biosolids, particularly Class B biosolids, contain a variety of human pathogenic viruses (Straub et al. 1993b). Sufficient viruses are normally present, so that sampling and detection are relatively simple. The choice of detection method is critical, however, when documenting the elimination of viruses. Standard-cell-culture methods for viruses in environmental samples are expensive and time consuming, requiring up to a month for confirmed positive results (Reynolds et al. 1997). Cell-culture assays are further complicated by the presence of toxic organic and inorganic materials found in sewage sludge. An alternative detection method is PCR, which, using specific oligonucleotide primers, relies on in vitro enzymatic amplification of target nucleic acids (Saiki et al. 1988). PCR analyses are quicker, less costly, and more sensitive than other cell-culture methods. Direct reverse transcriptase PCR (RT-PCR) can potentially detect intact nucleic acid sequences in viral protein coats, even when the viral particles have been inactivated. In that case, inactive viruses can be detected and the potential risk from their presence

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

overstated. PCR is positive for virus detection long after cell-culture results are negative.

The issue of virus viability versus virus detection with PCR has led to a debate on the efficacy of the PCR method. However, development of the integrated-cell-culture-PCR (ICC-PCR) has defused the debate (Reynolds et al. 1996). ICC-PCR combines biological amplification of viruses in cell culture and enzymatic amplification of viral RNA via PCR. There are many advantages to this method, particularly the prerequisite that the virus grow in cell culture for positive PCR amplification, thus detecting only viable viruses. A comparison of all three virus detection methods (Table 6–9) shows that for viral risk assessment analysis, ICC-PCR is the method of choice. Cell culture could potentially underestimate exposure, while RT-PCR could easily overestimate exposure.

Protozoa and Helminths

Over the past 20 years, various assays for helminth eggs in biosolids have been developed, but no assay has been universally accepted, primarily because there are few published quality-assurance and quality-control (QA-QC) data for the various protocols that have been used. Die-off studies with Ascaris eggs collected at different seasons showed that a consistent protocol for egg collection, storage, and use in spiking biosolids must be addressed. When such a protocol is developed, consistent QA-QC data can be obtained for helminth eggs spike studies (Reimers et al. 1981, 1986b, 1990). When detecting helminths, sample preservation and pretreatment is often overlooked. For Ascaris eggs, a neutralization and cooling process is necessary to assess the alkaline and acidic disinfection and stabilization of biosolids (Meehan et al. 1986). Several methods can be used to detect Ascaris eggs, including those of Bean and Brabants (2001a), Huyard et al. (2000), EPA (1999), and Yanko (1987). Each of those methods has a different percent recovery of eggs, and QA-QC data are available for only the Tulane Ascaris assay. The Tulane assay is accurate for anoxic and acidic biosolids at 75–80% with a precision of approximately 10–15%. A summary of the Tulane Ascaris assay is presented in Table 6–10.

This Ascaris assay gives no indication of QA-QC data relative to other helminth eggs or protozoa, and helminth eggs other than Ascaris are liable to require assay modifications. The process should work well for the eggs of the canine and feline ascarids Toxocara canis, Toxocara cati, and Toxascaris leonina which can enter wastestreams through toilets or storm runoff, because these eggs are slightly larger than the eggs of Ascaris and have similar densities. This method may not be as effective for eggs of the human whipworm Trichuris

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

TABLE 6–9 Comparisons of Methods for Detection of Virus

 

Method of Detection

Issue

Cell Culture

RT-PCR

ICC-PCR

Reduced time of detection

No

Yes

Yes

Infectious virus detected

Yes

Yes/No

Yes

Increased sensitivity

Yes

No

Yes

Affected by PCR inhibitory substances

No

Yes

No

Reduced costs

No

Yes

Yes

Detects only viable organisms

Yes

No

Yes

Detects viable but nonculturable virus

No

Yes

Yes

 

Source: Marlowe et al. 2000. Reprinted with permission from Environmental Microbiology; copyright 2000, Elsevier Science.

trichiura and the different human taeniid tapeworms. The technique is inappropriate for protozoa, because those of primary concern, Giardia and Cryptosporidium, will pass through the final sieve. Thus, for those pathogens, another form of final sample processing is required. At this time, the process described for Ascaris is good for verifying inactivation of pathogens in various spiked samples, but further work is required to verify recovery methods for routine samples when other pathogens are of equal or greater concern.

There is substantial concern over the reliability and accuracy of viability assays. Currently, the helminth egg assay for Ascaris is much more accurate, precise, and efficient than the Cryptosporidium oocyst assay, possibly because Cryptosporidium parvum is much more sensitive to temperature, cavitation, and noncharged biocidal constituents than Ascaris (Reimers et al. 1999). In general, Cryptosporidium can be inactivated with properly operated Class B disinfection, even though Cryptosporidium have been reported to survive Class B disinfection with lime stabilization (Bean and Brabants 2001b). In alkaline stabilization, the ammonia content generally controls the inactivation of helminth eggs and protozoan oocysts. Ascaris eggs require 1–3% ammonia for inactivation instead of the 0.1% required for Cryptosporidium. Cavitation is effective in inactivation of Cryptosporidium but is not as effective for Ascaris eggs, and the inactivation of Cryptosporidium occurs at 15°C less than that of Ascaris (Reimers et al. 1999; Bowman et al. 2000).

The preservation and pretreatment techniques for protozoan oocysts have not been developed to the level of those for helminth eggs. The viability and infectivity assays typically use one of the following techniques (Jakubowski et

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

TABLE 6–10 Summary of Tulane Ascaris Assay for Viability and Determination in Percent Recovery or Percent Variation from the Mean Density

Biosolids Matrix

% Recovery (Accuracy)

% Variation (Precision)

Reference

Acid treated

80.5–79.0

10.2–3.8

Reimers et al. 1991

Anaerobic digested and lagoon stored

75.5

14.8

Reimers et al. 1990

Soil blends

75.5

32.5

Leftwich et al. 1987

Alkaline treatment

58.5

34.4

Meehan et al. 1986

EPA White House document

<50.0

-

Bean and Brabants 2001a

In-vivo assay

<10.0

-

Burnham 1988

al. 1996): vital dye staining, animal infectivity, cell culture, or polymerase chain reactions (B-tubulin messenger RNA or RT-PCR). The animal viability assay would be useful for Cryptosporidium of human origin. Cell culture and mRNA testing also appear to have merit. Cryptosporidium recoveries from biosolids appear to be far less efficient than those from helminths, having a recovery efficiency of about 10% for the sedimentation technique and less than 3% for the flotation technique (Bean and Brabants 2001b). Recoveries of Cryptosporidium oocysts and Giardia cysts from biosolids varied from 3.2 to 16.3% and 2.4 to 41.7%, respectively. These data illustrate the need to optimize the techniques for protozoan preservation, pretreatment, and analysis, because recovery efficiencies vary, depending on the sampling matrix.

Potential Limitations in Dose-Response Information

One intrinsic feature of risk assessment is that the data used to define a dose-response relationship for both chemicals and microbial agents are most often obtained at relatively high doses. A mathematical relationship is then used to extrapolate the risk at lower exposure levels. It has long been known, however, that dose-response relationships may yield quite different low-dose risk levels (e.g., see Van Ryzin 1980). Thus, it is important to develop the appropriate specifications for plausible dose-response models for infectious microorganisms. Initial attempts at expressing such characteristics have been made (Holcomb et al. 1999). The two most successful models are the exponential and the beta-Poisson models, both of which express the risk at low

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

doses as a linear function of dose. This linear function has been demonstrated with outbreak data on Shigella and Giardia and with risks extrapolated from human volunteer trials (Crockett et al. 1996; Rose et al. 1991b).

A second important aspect of dose-response assessment is the relationship between the ingested dose and the severity and duration of effects. For some pathogens, the severity of the outcome depends on the initial ingested dose (Teunis et al. 1999). There may also be species and subspecies differences in infectivity (and in the severity of illness). Ideally, a dose-response relationship for the particular subspecies (or “strain”) should be obtained; however, that might not be possible in practice.

The differences in infectivity of different species of Salmonella and Shigella have been demonstrated (Crockett et al. 1996; Fazil 1996). Cryptosporidium parvum and different subspecies of E. coli manifest different dose-response relationships (Haas et al. 1999b; Okhuysen et al. 1999). Infectivity differences likely result from differences in pathogenicity. The degree to which biochemical markers may be used to predict infectivity quantitatively is an important research area.

A number of human dose-response relationships have been developed for bacteria, viruses, and protozoa (Regli et al. 1991; Rose et al. 1991b; Haas et al. 1993, 1996, 1999a; Crockett et al. 1996; Fazil 1996; Medema et al. 1996; Teunis et al. 1999). However, human or animal dose-response relationships for infection or illness from sewage sludge helminths (e.g., Ascaria, Tanenia) do not appear to have been identified.

Although it would be best to use human dose-response data, it is not possible for many organisms, and extrapolations must be made from animal studies. Studies on Listeria monocytogenes, a foodborne pathogen, and E. coli O157:H7 have used animal dose-response data to develop human dose-response information (Haas et al. 1999a, 2000). Exposures estimated from human infection rates during outbreaks were comparable to the estimated infection rate based on animal dose-response data, thus validating the use of animal data as a quantitative predictor of human response. However, such validation needs to be conducted in the case of each particular pathogen when an inference from animal dose-response information is to be made.

Protection of sensitive or susceptible subpopulations is frequently desired, although the definition of these subpopulations has not been rigorously defined. In a recent expert working group (Balbus et al. 2000), one definition was crafted: e”Susceptibility is a capacity characterizable by a set of intrinsic and extrinsic factors that modify the impacts of a specific exposure upon risks/severity of outcomes in an individual or population.” Under that definition, susceptible subpopulations could include the immunocompromised (including HIV-infected persons and persons taking immunosuppressive

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

drugs), pregnant women, the elderly, and children (Gerba et al. 1996). In addition, susceptible subpopulations could include persons with less access to health care or with concomitant factors, such as diet or use of illicit drugs, which might enhance risk or infectivity. As yet, there is no validated way to incorporate altered susceptibility for infectious microorganisms into a risk assessment. Such incorporation will probably require animal models to assess dose-response alterations associated with differing susceptibility.

Exposure Routes Other Than Ingestion

Microbial risk assessment is usually based on ingestion of contaminated food or water; however, biosolids exposure might occur by inhalation or direct dermal contact. Outbreak reports suggest that microorganisms found in biosolids might be transmitted by inhalation (Giubileo et al. 1998; Gregersen et al. 1999; Marks et al. 2000). Dose-response relationships and exposure models for these microorganisms are needed. In some cases, for example, for pathogenic fungi, there are no ingestion analogs on which to base infectivity via inhalation. Some animal models have been developed for inhalation exposure to biotoxins (including bacterial endotoxins and other microbial inflammatory agents) (Thorne 2000). A research program is needed to develop methods for the risk assessment of these agents.

Population Level Modeling

Two considerations of pathogen risk assessment that have no analog in chemical risk assessment is the need to address the potential for secondary transmission and acquired immunity. Secondary cases of infection may arise by a variety of mechanisms, such as transmission among close family members. Household secondary cases can arise by direct or indirect (e.g., surface contamination) contact, particularly when the primary case or one household secondary case is a child (Heun et al. 1987; Griffin and Tauxe 1991; Mac Kenzie et al. 1995). Presumably, secondary cases may also arise from close contact with an asymptomatic individual (in the “carrier” state). This is wellknown for highly acute and now uncommon illnesses, such as typhoid. Excretion of Norwalk virus following recovery and resulting in additional cases has been documented to occur for as long as 48 h after recovery (White et al. 1986).

There is evidence that transmission of organisms, at least for some illnesses, may occur before as well as after symptoms appear. In studying day-care rotavirus infections, Pickering et al. (1988) noted that more than 10% of

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

the children excreted rotavirus up to 5 days before the onset of symptomatic illness. This pre-symptom excretion of rotavirus represents one route of transmission.

The impact of secondary infections may be considered in at least two ways. A first approximation may be made by multiplying the estimated number of primary cases by a secondary-case ratio. A second estimate may be made by using population-based models, as discussed in Chapter 7. These models have been documented in a number of reports (e.g., Eisenberg et al. 1996, 1998; Haas et al. 1999b). However, the models are still at the research stage, as certain parameters (e.g., incubation time, duration and intensity of immunity, and effectiveness of person-to-person contact) are poorly characterized for waterborne diseases. Furthermore, there might be an underlying endemic baseline of illness on which an outbreak can be superimposed (Morris et al. 1998). As additional data become available, it might be possible for population-based risk assessments to assess the impact of control options for infectious organisms.

FINDINGS AND RECOMMENDATIONS

The pathogen standards of the Part 503 rule are technologically based requirements intended to reduce the presence of pathogens. The standards consist of treatment, use, and monitoring requirements. Classification of Class A and Class B biosolids are based largely on fecal coliforms as indicator organisms. Class A biosolids do not have detectable concentrations of pathogens (determined by indicator organisms) and, therefore, risks from them are expected to be lower than those from Class B. Pathogens are normally present in Class B biosolids, but the risk they pose is unknown, because no risk assessment has been performed.

In determining the pathogen standards for biosolids, EPA considered a variety of potential bacteria, viruses, protozoa, and helminths that might be present in biosolids, their fate and transport in the environment, and the potential for human contact. The committee found that EPA considered an appropriate spectrum of pathogens and indicator organisms in setting its standards, but new information on those and other pathogens not considered is now available for conducting a national sewage sludge survey of pathogens and updating hazard identification. Because of the variety of pathogens that have the potential to be in biosolids, the committee supports EPA’s use of pathogen-reduction requirements, use restrictions, and monitoring of indicator organisms, rather than pathogen-specific concentration limits, in its regulations.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

Recommendations:

  • EPA should conduct a national survey of pathogen occurrence in raw and treated sewage sludges. Important elements in conducting the survey include use of consistent sampling methods, analysis of a broad spectrum of pathogens that could be in sewage sludge, and use of the best available (preferably validated) pathogen measurement techniques.

  • Additional indicator organisms, such as Clostridium perfringens, should be considered for potential use in regulation of land-applied biosolids. Such indicators and other operational parameters (e.g., time, temperature, pH, and chemical dose) may be suitable for assessing day-to-day compliance with the regulations.

As with the chemical standards, EPA based its pathogen standards on selected pathogens and exposure conditions that were expected to be representative and conservative enough to be applicable to all areas of the United States and for all types of land applications. However, pathogen survival in soils may range from hours to years, depending on the specific pathogens, biosolids-application methods and rates, initial pathogen concentrations, soil composition, and meteorological and geological conditions. In addition, very few data are available to estimate the occurrence, transport, and decay rates of pathogens and endotoxins in bioaerosols.

Recommendation: Site restrictions, buffer zones, and holding periods for land-applied Class B biosolids should consider geographic and site-specific conditions that affect pathogen fate and transport.

Regulations for Class B biosolids include use restrictions. These restrictions are intended to limit animal and human contact with land-applied biosolids until environmental factors reduce pathogens to concentrations that are not expected to cause adverse effects. Because there are no requirements for on-site monitoring of pathogens, there is little information available to evaluate the reliability of use restrictions in achieving their intended minimum exposure levels or to verify that those desired levels are maintained over an extended time.

In addition, the committee found that some potential exposure pathways were not sufficiently considered when the use restrictions were developed. For example, potential off-site inhalation of dust and aerosols does not appear to have been considered. The potential for groundwater contamination by pathogens was not sufficiently addressed. This is a concern in geologically sensitive areas, where there is the potential for leachate from application sites to contaminate subsurface-water resources. In addition, the potential for runoff to contaminate surface waters was not adequately addressed.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

Recommendations:

  • Studies should be conducted to determine whether the site restrictions specified for Class B biosolids in the Part 503 rule actually achieve their intended effect with regard to pathogen levels.

  • As recommended in Chapter 5 for chemicals, EPA should develop a conceptual site model to identify the major and minor exposure pathways (including secondary transmission) by which humans might come into contact with pathogens in biosolids.

Substantial advances in detection and quantification of pathogens in the environment have been made since the promulgation of the Part 503 rule. For example, new molecular techniques for detecting pathogens, such as PCR, are now available. In addition, new approaches to environmental sample collection and processing are available. However, no consensus standards have been developed for pathogen measurements in biosolids and bioaerosols.

Recommendation: EPA should foster development of standardized methods for measurement of pathogens in biosolids and bioaerosols. EPA should include round-robin laboratory testing to establish method accuracies and precisions at the various pathogen concentrations expected in raw sewage sludge and partially and fully treated biosolids. These new detection methods should be used to verify that EPA’s prescribed pathogen reduction techniques are reliable in achieving their intended goals. Mechanisms should be developed for incorporating new methodologies into the verification process as they become available.

Microbial risk-assessment methods similar to those used in chemical risk assessments have been developed for pathogens in drinking water and food. These methods are not as well-established as those for chemicals, and there are important differences between the two. For example, a microbial risk assessment must include the possibility of secondary infections, either through person-to-person contact or from transmission of the pathogen to others through air, food, or water. The importance of secondary transmission depends in part on the level of acquired immunity to the pathogen in the community, a phenomenon that has no analog in chemical risk assessment.

The committee believes quantitative microbial risk assessment (QMRA) is a feasible approach to setting standards for pathogens in biosolids. The committee does not recommend that QMRA be used to establish pathogen-specific regulatory concentration limits but recommends that it be used as a tool for developing treatment, use, and monitoring requirements (or for validating current requirements) to meet acceptable risk levels. However, there are still substantial data gaps, such as characterization of dose-response relationships and transport and fate of pathogens and endotoxins in biosolids and

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

bioaerosols. Monitoring of compliance with the regulations should continue to be conducted using indicator organisms and operational parameters and practices (e.g., temperature, buffer zones, and pH) to ensure that tolerable risk levels are not exceeded.

Recommendation: QMRAs should be developed and used to establish (or validate) regulatory criteria (treatment processes, use restrictions, and monitoring) for pathogens in biosolids. They can also be used for sensitivity analyses and identifying critical information that is needed to reduce uncertainty about the risks from pathogens in biosolids. To conduct these risk assessments, consideration must be given to assessing risks from all potential routes of exposure (e.g., bioaerosols, groundwater), dose-response relationships, pathogen survival, and secondary transmission of disease. In some cases, research will be needed to fill gaps in knowledge of those inputs. As additional information is gathered on exposure, dose-response relationship, and pathogen survival, the risk assessments should be reviewed and updated as necessary.

REFERENCES

al-Ghazali, M.R., and S.K.al-Azawi. 1990. Listeria monocytogenes contamination of crops grown on soil treated with sewage sludge cake. J. Appl. Bacteriol. 69(6):642–647.

Alvarez, A.J., M.P.Buttner, and L.D.Stetzenbach. 1995. PCR for bioaerosol monitoring: Sensitivity and environmental interference. Appl. Environ. Microbiol. 61(10):3639–3644.

Anderson, R.M., and R.M.May. 1991. Infectious Diseases in Humans: Dynamics and Control. Oxford: Oxford University Press.

Arana, I., J.I.Justo, A.Muela, and I.Barcina. 2001. Survival and plasmid transfer ability of Escherichia coli in wastewater. Water Air Soil Pollut. 126(3/4):223–238.

Arrowood, M.J. 1995. Assessment of Pulse Power System to Inactivate Cryptosporidium parvum oocysts. Report to Scientific Utilization, Inc., Huntsville, AL, by Centers for Disease Control, Atlanta, GA. January 11, 1995.

Ashbolt, N.J., G.S.Grohmann, and C.S.W.Kueh. 1993. Significance of specific bacterial pathogens in the assessment of polluted receiving waters of Sydney, Australia. Water Sci. Technol. 27(3–4):449–452.

ASTM (American Society for Testing and Materials). 2001. E884–82(2001) Standard Practice for Sampling Airborne Microorganisms at Municipal Solid-Waste Processing Facilities. American Society for Testing and Materials, West Conshohocken, PA.

Ayres, R.M., D.L.Lee, D.D.Mara, and S.A.Silva. 1993. The accumulation, distribution and viability of human parasitic nematode eggs in the sludge of a primary

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

facultative waste stabilization pond

. Trans. R. Soc. Trop. Med. Hyg. 87(3):256– 258.

Balbus, J., R.Parkin, and M.Embrey. 2000. Susceptibility in microbial risk assessment: Definitions and research needs. Environ. Health Perspect 108(9):901–905.

Barbier, D., D.Perrine, C.Duhamel, R.Doublet, and P.Georges. 1990. Parasitic hazard with sewage sludge applied to land. Appl. Environ. Microbiol. 56(5):1420–1422.

Bailey, N.T.J. 1975. The Mathematical Theory of Infectious Diseases and Its Applications, 2nd Ed. New York: Oxford University Press.

Bale Jr. J.F. 2000. Cysticercosis. Curr. Treat. Options Neurol. 2(4):355–360.

Bean, C.L., and J.J.Brabants. 2001a. Lab analyzes Ascaris ova recovery rates using revised protocols. Biosolids Technical Bulletin 7(1):12–14.

Bean, C.L., and J.J.Brabants. 2001b. A Survey of Wastewater Solids to Assess the Prevalence of Cryptosporidium, Giardia Species, and Ascaris lumbricoides: An Evaluation of Risks Associated with Land Application of Biosolids. Poster presented at the 101st General Meeting of the American Society of Microbiology, Orlando, FL. May 23, 2001.

Bitton, G., O.C.Pancorbo, and S.R.Farrah. 1984. Virus transport and survival after land application of sewage sludge. Appl. Environ. Microbiol. 47(5):905–909.

Blanker, E.M., M.D.Little, R.S.Reimers, and T.G.Akers. 1992. Evaluating the use of Clostridium perfringens spores as indicator of the presence of viable Ascaris eggs in chemically treated municipal sludges. Pp. 201–215 in The Future Direction of Municipal Sludge (Biosolids) Management: Where We Are and Where We’re Going, Proceedings, Specialty Conference, Portland, OR, July 26–30, 1992, Vol. 1. Portland, OR: Water Environment Federation.

Blumenthal, U.J., D.D.Mara, A.Peasey, G.Ruiz-Palacios, and R.Stott 2000. Guidelines for the microbiological quality of treated wastewater used in agriculture: Recommendations for revising WHO guidelines. Bull. World Health Organ. 78(9):1104–1116.

Bottcher, R.W. 1998. Dust in livestock and poultry buildings: Health effects, interactions with odors, and control options. In: Schiffman, S.S., Walker, J.M., Small, R., Millner, P. (Organizing Committee). Participant Reviews and Opinions: Workshop on Health Effects of Odors, Duke University, 1998. (Cited in Schiffman et al. 2000).

Bowman, D.D., R.S.Reimers, M.D.Little, M.B.Jenkins, W.S.Bankston, and M.M. Atique. 2000. Assessment and Comparison of Ascaris Egg and Cryptosporidium Oocyst Inactivation With Respect to Biosolids Processing. 14th Annual Residuals and Biosolids Management Conference, February/March 2000. Specialty Conf. Paper. Water Environment Federation, Alexandria, VA.

Brenner, K.P., P.V.Scarpino, and S.C.Clark. 1988. Animal viruses, coliphages and bacteria in aerosols and wastewater at a spray irrigation site. Appl. Environ. Microbiol. 54(2):409–415.

Brown, L.M. 2000. Helicobacter pylori: Epidemiology and routes of transmission. Epidemiol. Rev. 22(2):283–297.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

Bujoczek, G. 2001. Influence of Ammonia and Other Abiotic Factors on Microbial Activity and Pathogen Inactivation During Processing of High-Solid Residues. Ph.D. Dissertation. University of Manitoba, Winnipeg, MB, Canada.

Bünger, J., M.Antlauf-Lammers, T.G.Schulz, G.A.Westphal, M.M.Müller, P. Ruhnau, and E.Hallier. 2000. Health complaints and immunological markers of exposure to bioaerosols among biowaste collectors and compost workers. Occup. Environ. Med. 57(7):458–464.

Burnham J.C. 1988. The alkaline stabilization and disinfection of municipal wastewater sludge, Toledo, Ohio. A Case of Governmental, Business and Academic Cooperation. Pp. 112–123 in Residuals Management, Proceedings of Residuals Management Specialty Conference, Atlanta, GA, April 19–20, 1988. Alexandria, VA: Water Pollution Control Federation.

Butterfield, J., J.C.Coulson, S.V.Kearsey, P.Monaghan, J.H.McCoy, and G.E.Spain. 1983. The herring gull Larus argentatus as a carrier of salmonella. J. Hyg. (Lond). 91(3):429–436.

Carlson, D.B., and R.L.Knight. 1987. Mosquito production and hydrological capacity of southeast Florida impoundments used for wastewater retention. J. Am. Mosq. Control Assoc. 3(1):74–83.

Casanova, L.M., C.P.Gerba, and M.Karpiscak. 2001. Chemical and microbial characteristics of household graywater. J. Environ. Sci. Health Part A 36(4):395–402.

Chappell, C.L., P.C.Okhuysen, C.R.Sterling, C.Wang, W.Jakubowski, and H.L. Dupont. 1999. Infectivity of Cryptosporidium parvum in healthy adults with pre-existing anti-C parvum serum immunoglobulin G. Am. J. Trop. Med. Hyg. 60(1):157–164.

Chapron, C.D., N.A.Ballester, and A.B.Margolin. 2000. The detection of astrovirus in sludge biosolids using an integrated cell culture nested PCR technique. J. Appl. Microbiol. 89(1):11–15.

Chauret, C., S.Springthorpe, and S.Sattar. 1999. Fate of Cryptosporidium oocysts, Giardia cysts, and microbial inidicators during wastewater treatment and anaerobic sludge digestion. Can. J. Microbiol. 45(3):257–262.

Chee-Sanford,J.C., R.I.Aminov, I.J.Krapac, N.Garrigues-Jeanjean, and R.I.Mackie. 2001. Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine production facilities. Appl. Environ. Microbiol. 67(4):1494–1502.

Coleman, M., and H.Marks. 1998. Topics in dose-response modeling. J. Food Prot. 61(11):1550–1559.

Cook, M.B., and J.A.Hanlon. 1993. The role of the pathogen equivalency committee under the Part 503 standards for the use or disposal of sewage sludge. Memorandum to Water Division Directors, Regions I–X, from Michael B.Cook, Director, Office of Wastewater Enforcement and James A.Hanlon, Acting Director, Office of Science and Technology, Washington, DC, dated June 15, 1993. Pp. 62–65 in Environmental Regulations and Technology, Control of Pathogens and Vector Attraction in Sewage Sludge. EPA/625/R-92/013. Office of Research and Development, U.S. Environmental Protection Agency, Washington, DC.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

Cooperative State Research Service Technical Committee W-170. 1989. Peer Review, Standards for the Disposal of Sewage Sludge, U.S. EPA Proposed Rule 40 CFR Parts-257 and 503 (February 6, 1989 Federal Register pp. 5746–5902). Submitted to William R.Diamond, Criteria and Standards Division, U.S. Environmental Protection Agency. Washington, DC: U.S. Dept. of Agriculture, Cooperative State Research Service.

Cotte, L., M.Rabodonirina, F.Chapuis, F.Bailly, F.Bissuel, C.Raynal, P.Gelas, F. Persar, M.A. Piens, and C.Trepo. 1999. Waterborne outbreak of intestinal microsporifiosis in persons with and without human immunoodeficiency virus infection. J. Infect Dis. 180(6):2003–2008.

Cox, C.S. 1987. The Aerobiological Pathway of Microorganisms. Chichester: Wiley.

Croci, L., M.Ciccozzi, D.De Medici, S.DiPasquale, A.Fiore, A.Mele, and L.Toti. 1999. Inactivation of hepatitis A virus in heat-treated mussels. J. Appl. Microbiol. 87(6):884–888.

Crockett, C.S., C.N.Haas, A.Fazil, J.B.Rose, and C.P.Gerba. 1996. Prevalence of shigellosis in the U.S.: Consistency with dose-response Information. Int. J. Food Microbiol. 30(1–2):87–99.

Damgaard-Larsen, S., K.O.Jensen, E.Lund, and B.Nissen. 1977. Survival and movement of enterovirus in connection with land disposal of sludges. Water Res. 11(6):503–509.

Dawson, S., F.McArdle, D.Bennett, S.D.Carter, M.Bennett, R.Ryvar, and R.M. Gaskell. 1993. Investigation of vaccine reactions and breakdowns after feline calicivirus vaccination. Vet. Rec. 132(16):346–350.

DeLuca, G., F.Zanetti, P.Fateh-Moghadm, and S.Stampi. 1998. Occurrence of Listeria monocytogenes in sewage sludge. Zentralbl. Hyg. Umweeltmed. 201(3):269–277.

Deneen, V.C., J.M. Hunt, C.R.Paule, R.I.James, R.G.Johnson, M.J.Raymond, and C.W.Hedberg. 2000. The impact of foodborne calicivirus disease: The Minnesota experience. J. Infect. Dis. 181(Suppl. 2):S281–283.

De Serres, G., and D.Laliberté. 1997. Hepatitis A among workers from a waste water treatment plant during a small community outbreak. Occup. Environ. Med. 54(1):60–62.

Dowd, S.E., and R.M.Maier. 2000. Aeromicrobiology. Pp. 91–122 in Environmental Microbiology, R.M.Maier, I.L.Pepper, and C.P.Gerba, eds. San Diego: Academic Press.

Dowd, S.E., and S.D.Pillai. 1999. Identifying the sources of biosolids derived pathogen indicator organisms in aerosols by ribosomal DNA fingerprinting. J. Environ. Sci. Health-A 34(5):1061–1074.

Dowd, S.E., C.P.Gerba, I.L.Pepper, and S.D.Pillai. 2000. Bioaerosol transport modeling and risk assessment in relation to biosolid placement. J. Environ. Qual. 29(1):343–348.

Dowd, S.E., S.D.Pillai, S.Wang, and M.Y.Corapcioglu. 1998. Delineating the specific influence of virus isoelectric point and size on virus adsorption and transport through sandy soils. Appl. Environ. Microbiol. 64(2):405–410.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

Dowd, S.E., K.W.Widmer, and S.D.Pillai. 1997. Thermotolerant clostridia as an airborne pathogen indicator during land application of biosolids. J. Environ. Qual. 26(1):194–199.

Droffner, M.L., and W.F.Brinton. 1995. Survival of E. coli and Salmonella populations in aerobic thermophilic composts as measured with DNA gene probes. Zentralbl. Hyg. Umweltmed. 197(5):387–397.

Eduard, W. 1996. Measurement methods and strategies for non-infectious microbial components in bioaerosols at the workplace. Analyst 121(9):1197–1201.

Eduard, W., and D.Heederick. 1998. Methods for quantitative assessment of airborne levels of noninfectious microorganisms in highly contaminated work environments. Am. Ind. Hyg. Assoc. J. 59(2):113–127.

Eisenberg, J.N., E.Y.Seto, A.W.Olivieri and R.C.Spear. 1996. Quantifying water pathogen risk in an epidemiological framework. Risk Anal. 16(4):549–563.

Eisenberg, J.N., E.Y.Seto, J.M.Colford Jr., A.W.Olivieri, and R.C.Spear. 1998. An analysis of the Milwaukee cryptosporidiosis outbreak based on a dynamic model of the infection process. Epidemiology 9(3):255–263.

Enriquez, C.E., C.J.Hurst, and C.P.Gerba. 1995. Survival of the enteric adenoviruses 40 and 41 in tap, sea, and wastewater. Wat. Res. 29(11):2548–2553.

EPA (U.S. Environmental Protection Agency). 1991a. Preliminary Risk Assessment for Parasites in Municipal Sewage Sludge Applied to Land. EPA/600/6–91/001. Office of Research and Development, U.S. Environmental Protection Agency. Washington, DC. March 1991.

EPA (U.S. Environmental Protection Agency). 1991b. Preliminary Risk Assessment for Bacteria in Municipal Sewage Sludge Applied to Land. EPA/600/6–91/006. Office of Research and Development, U.S. Environmental Protection Agency, Washington, DC. July 1991.

EPA (U.S. Environmental Protection Agency). 1992. Preliminary Risk Assessment for Viruses in Municipal Sewage Sludge Applied to Land. EPA/600/R-92/064. Office of Research and Development, U.S. Environmental Protection Agency, Washington, DC. June 1992.

EPA (U.S. Environmental Protection Agency). 1993. Federal Register: February 19, 1993. 40 CFR Parts 257, 403, and 503. The Standards for the Use or Disposal of Sewage Sludge. Final Rules. EPA 822/Z-93/001. U.S. Environmental Protection Agency.

EPA (U.S. Environmental Protection Agency). 1999. Environmental Regulations and Technology: Control of Pathogens and Vector Attraction in Sewage Sludge. EPA/625/R-92/013. Office of Research and Development, U.S. Environmental Protection Agency, Washington DC. [Online]. Available: http://www.epa.gov/ttbnrmrl/625/R-92/013.htm [January 4, 2002].

EPA (U.S. Environmental Protection Agency). 2001. Workshop on Emerging Infectious Disease Agents and Associated With Animal Manures, Biosolids and Other Similar By-Products, Cincinnati, OH, June 4–6, 2001. National Risk Management Research Laboratory, U.S. Environmental Protection Agency, Cincinnati, OH.

Evans, D.A., and W.L.Puskas. 1986. Application of ultrasound for disinfection and pasteurization. Pp. 259–268 in Applied Fields for Energy Conservation, Water

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

Treatment, and Industrial Applications, Final Report, R.S.Reimers, S.F.Bock, and L.E.White, eds. DOE/CE/40568-T1 (DE86014306). Washington, DC: Technical Information Center, Office of Scientific and Technical Information, U.S. Dept. of Energy. June 1986.

Fazil, A.M. 1996. A Quantitative Risk Assessment Model for Salmonella. M.S. Thesis, Drexel University, Philadelphia, PA.

Feachem, R.G., D.J.Bradley, and H.Garelick. 1983. Sanitation and Disease: Health Aspects of Excreta and Waste Management. New York: Wiley.

FSIS (Food Safety and Inspection Service). 1998a. Salmonella Enteritidis Risk Assessment: Shell eggs and egg products. Food Safety and Inspection Service, U.S. Department of Agriculture, Washington, DC. [Online]. Available: http://www.fsis.usda.gov/ophs/risk/index.htm [January 4, 2002].

FSIS (Food Safety and Inspection Service). 1998b. Risk assessment of E. coli O157:H7 in ground beef. Food Safety and Inspection Service, U.S. Department of Agriculture, Washington, DC. [Online]. Available: http://www.fsis.usda.gov/OPHS/ecolrisk/home.htm [January 4, 2002].


Gavett, S.H., and H.S.Koren. 2001. The role of particulate matter in exacerbation of atopic asthma. Int. Arch. Allergy Immunol. 124(1–3):109–112.

George, C.L., H.Jin, C.L.Wohlford-Lenane, M.E.O’Neill, J.C.Phipps, P. O’Shaughnessy, J.N.Kline, P.S.Thorne, and D.A.Schwartz. 2001. Endotoxin responsiveness and subchronic grain dust-induced airway disease. Am. J. Physiol. Lung Cell Mol. Physiol. 280(2):L203–213.

Gerba, C.P., and J.B.Rose. 1990. Viruses in source and drinking water. Pp. 380–396 in Drinking Water Microbiology: Progress and Recent Developments, G.A. McFeters, ed. New York: Springer-Verlag.

Gerba, C.P., C.Wallis, and J.L.Melnick. 1975. Fate of wastewater bacteria and viruses in soil. Proc. ASCE J. Irrig. Drain. Div. 101:157–174.

Gerba, C.P., J.B.Rose, and C.N.Haas. 1996. Sensitive populations: Who is at the greatest risk? Int. J. Food Microbiol. 30(1–2): 113–123.

Gibbs, R.A., C.J.Hu, G.E.Ho, and I.Unkovich. 1997. Regrowth of faecal coliforms and salmonellae in stored biosolids and soil amended with biosolids. Water Sci. Technol. 35(11):269–275.

Giubileo, L., A.M.Sarti, L.A.Bianchi, E.Calcaterra and A.Colombi. 1998. Review of risks of biological agents and preventive measures to safeguard the health of compost production workers, [in Italian]. Med. Lav. 89(4):301–315.

Godfree, A. 2001. Control of pathogens. Workshop on Emerging Infectious Disease Agents and Associated With Animal Manures, Biosolids and Other Similar By-Products, Cincinnati, OH, June 4–6, 2001, National Risk Management Research Laboratory, U.S. Environmental Protection Agency, Cincinnati, OH.

Goyal, S.M., and C.P.Gerba. 1979. Comparative adsorption of human enteroviruses, simian rotavirus and selected bacteriophages to soils. Appl. Environ. Microbiol. 38(2):241–247.

Green, K.Y., T.Ando, M.S.Balayan, T.Berke, I.N.Clarke, M.K.Estes, D.O.Matson, S.Nakata, J.D.Neill, M.J.Studdert, and H-J.Thiel. 2000. Taxonomy of the caliciviruses. J. Infect. Dis. 181(Suppl 2):S322–330.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

Gregersen, P., K.Grunnet, S.A.Uldum, B.H.Andersen, and H.Madsen. 1999. Pontiac fever at a sewage treatment plant in the food industry. Scand. J. Work Environ. Health 25(3):291–295.

Gregory, J. 1994. Cryptosporidium in water: Treatment and monitoring methods. Filtr. Sep. 31(3):283–289.

Griffin, P.M., and R.V.Tauxe. 1991. The epidemiology of infections caused by Escherichia coli O157:H7, other enterohemorrhagic E. coli and the associated hemolytic uremic syndrome. Epidemiol. Rev. 13:60–98.

Grubel, P., J.S.Hoffman, F.K.Chong, N.A.Burstein, C.Mepani, and D.R.Cave. 1997. Vector potential of houseflies (Musca domestica) for Helicobacter pylori. J. Clin. Microbiol. 35(6):1300–1303.

Haas, C.N., J.B.Rose, C.Gerba, and S.Regli. 1993. Risk assessment of virus in drinking water. Risk Anal. 13(5):545–552.

Haas, C.N., C.S.Crockett, J.B.Rose, C.Gerba, and A.Fazil. 1996. Assessing the risk posed by oocysts in drinking water. Am. Water Works Assoc. J. 88(9):131–136.

Haas, C.N., J.B.Rose, and C.P.Gerba. 1999b. Quantitative Microbial Risk Assessment. New York: Wiley.

Haas, C.N., A.Thayyar-Madabusi, J.B.Rose, and C.P.Gerba. 1999a. Development and validation of dose response relationship for Listeria monocytogenes. Quant. Microbiol. 1(1):89–102.

Haas, C.N., A.Thayyar-Madabusi, J.B.Rose, and C.P.Gerba. 2000. Development of a dose-response relationship for Escherichia coli O157:H7. Int. J. Food Microbiol. 56(2–3):153–159.

Hegarty, J.P., M.T.Dowd, and K.H.Baker. 1999. Occurrence of Helicobacter pylori in surface water in the United States. J. Appl. Microbiol. 87(5):697–701.

Hess, E., and C.Breer. 1975. Epidemiology of salmonellae and fertilizing of grass-land with sewage sludge, [in German]. Zentralbl. Bakteriol. 161(1):54–60.

Heun, E.M., R.L.Vogt, P.J.Hudson, S.Parren, and G.W.Gary. 1987. Risk factors for secondary transmission in households after a common-source outbreak of Norwalk gastroenteritis. Am. J. Epidemiol. 126(6):1181–1186.

Hirsch, R., T.Ternes, K.Haberer, and K.L.Kratz. 1999. Occurrence of antibiotics in the aquatic environment. Sci. Total Environ. 225(1–2):109–118.

Holcomb, D.L., M.A.Smith, G.O.Ware, Y.C.Hung, R.E.Brackett, and M.P.Doyle. 1999. Comparison of six dose-response models for use with food-borne pathogens. Risk Anal. 19(6):1091–1100.

Hollander, A., D.Heederick, P.Versloot, and J.Douwes. 1993. Inhibition and enhancement in the analysis of airborne endotoxin levels in various occupational environments. Am. Ind. Hyg. Assoc. J. 54(11):647–653.

Huang, P.W., D.Laborde, V.R.Land, D.O.Matson, A.W.Smith, and X.Jiang. 2000. Concentration and detection of caliciviruses in water samples by reverse transcription-PCR. Appl. Environ. Microbiol. 66(10):4383–4388.

Hugh-Jones, M.E., and P.B.Wright. 1970. Studies on the 1967–8 foot-and-mouth disease epidemics: The relation of weather to the spread of disease. J. Hyg. 68(2):253–271.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

Huyard, A., B.Ferran, and J.M.Audic. 2000. The two phase anaerobic digestion process: Sludge stabilization and pathogens reduction. Water Sci. Technol. 42(9):41–48.

Ivens, U.I., N.O.Breum, N.Ebbehoj, B.H.Nielsen, O.M.Poulsen, and H.Wurtz. 1999. Exposure-response relationship between gastrointestinal problems among waste collectors and bioaerosols exposure. Scand. J. Work Environ. Health. 25(3):238–245.

ILSI Risk Science Institute Pathogen Risk Assessment Working Group. 1996. A conceptual framework to assess the risks of human disease following exposure to pathogens. Risk Anal. 16(6):841–848.


Jakubowski, W., S.Boutros, W.Faber, R.Payer, W.Ghiorse, M.LeChevallier, J.Rose, S.Schaub, A.Singh, and M.Stewart. 1996. Environmental methods for Cryptosporidium. Am. Water Works Assoc. J. 88(9):107–121.

Jenkins, M.B., M.J.Walker, D.D.Bowman, L.C.Anthony, and W.C.Ghiorse. 1999. Use of a sentinel system for field measurements of Cryptosporidium parvum oocyst inactivation in soil and animal waste. Appl. Environ. Microbiol. 65(5):1998–2005.

Juozaitis, A., K.Willeke, S.A.Grinshpun, and J.A.Donelly. 1994. Impaction onto a glass slide or agar versus impingement into a liquid for the collection and recovery of airborne microorganisms. Appl. Environ. Microbiol. 60(3):861–870.

Juris, P., I.Vilagiova, and P.Plachy. 1995. The importance of flies (Diptera-Brachycera) in the dissemination of helminth eggs from sewage treatment plants, [in Slovak]. Vet. Med. (Praha) 40(9):289–292.


Koudela, B., S.Kucerova, and T.Hudcovic. 1999. Effect of low and high temperatures on infectivity of Encephalitozoon cuniculi spores suspended in water. Folia Parasitol. 46(3):171–174.

Kukkula, M., P.Arstila, M.L.Klossner, L.Maunula, C.H.Bonsdorff, and P.Jaatinen. 1997. Waterborne outbreak of viral gastroenteritis. Scand. J. Infect Dis. 29(4):415–418.


Lacey, J., and B.Crook. 1988. Fungal and actinomycete spores as pollutants of the workplace and occupational allergens. Ann. Occup. Hyg. 32(4):515–533.

Lawrence, J.G., and H.Ochman. 1998. Molecular archaeology of the Escherichia coli genome. Proc. Natl. Acad. Sci. USA 95(16):9413–9417.

Learner, M.A. 2000. Egression of flies from sewage filter-beds. Water Res. 34(3):877–889.

Leftwich, D.B., D.B.George, R.S.Reimers, M.D.Little, and N.A.Klein. 1987. A Field Investigation of Ascaris Ova Survival in Domestic Sludge Applied to Land. Draft Report. Prepared to U.S. Environmental Protection Agency by LCC Institute of Water Research, Lubbock, TX.

Lembke, L.L., R.N.Kniseley, R.C.Van Nostrand, and M.D.Hale. 1981. Precision of the all glass impinger and the Andersen microbial impactor for air sampling in solid waste facilities. Appl. Environ. Microbiol. 42(2):222–225.

Leong, L.Y.C. 1983. Removal and Inactivation of viruses by treatment processes for potable water and wastewater: A review. Water Sci. Technol. 15:91–114.

Lever, R. 1996. Infection in atopic dermatitis. Derm. Ther. 1:32–37.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

Lighthart, B., and A.S.Frisch. 1976. Estimation of viable airborne microbes downwind from a point source. Appl. Environ. Microbiol. 31(5):700–704.

Lighthart, B., and A.J.Mohr. 1987. Estimating downwind concentrations of viable airborne microorganisms in dynamic atmospheric conditions. Appl. Environ. Microbiol. 53(7):1580–1583.

Lighthart, B., and B.T.Shaffer. 1995. Airborne bacteria in the atmospheric surface layer: temporal distribution above a grass seed field. Appl. Environ. Microbiol. 61(4):1492–1496.

Lighthart, B., and L.D.Stetzenbach. 1994. Distribution of microbial bioaerosol. Pp. 68–98 in Atmospheric Microbial Aerosols: Theory and Applications, B. Lighthart, and A.J.Mohr, eds. New York: Chapman & Hall.

Lindqvist, R., and A.Westoo. 2000. Quantitative risk assessment for Listeria monocytogenes in smoked or gravad salmon and rainbow trout in Sweden. Int. J. Food Microbiol. 58(3):181–196.

Liu, A.H., and A.H.Redmon, Jr. 2001. Endotoxin: Friend or foe? Allergy Asthma Proc. 22(6):337–340.

Lue-Hing, C., S.J.Sedita, P.Tata, J.J.Bertucci, C.R.Kambhampati, D.R.Zenz, and G.J.Knafl. 1998. Final Report on Certification of the Sludge Processing Trains (SPTS) of the Metropolitan Water Reclamation District of Greater Chicago (District) as Equivalent to Process to Further Reduce Pathogens. Submitted to Pathogen Equivalency Committee (PEC), U.S. Environmental Protection Agency by Metropolitan Water Reclamation District of Greater Chicago, Chicago, IL.

Lytle, D.A., E.W.Rice, C.H.Johnson, and K.R.Fox. 1999. Electrophoretic mobilities of Escherichia coli 0157:H7 and wild-type Escherichia coli strains. Appl. Environ. Microbiol. 65(7):3222–3225.

MacKenzie, W.R., W.L.Schell, B.A.Blair, D.G.Addiss, D.E.Peterson, N.J.Hoxie, J.J.Kazmierczak, and J.P.Davis. 1995. Massive outbreak of waterborne cryptosporidium infection in Milwaukee, Wisconsin: Recurrence of illness and risk of secondary transmission. Clin. Infect. Dis. 21(1):57–62.

Marks, H.M., M.E.Coleman, C.T.Lin, and T.Roberts. 1998. Topics in microbial risk assessment: Dynamic flow tree process. Risk Anal. 18(3):309–328.

Marks, P.J., I.B.Vipond, D.Carlisle, D.Deakin, R.E.Fey, and E.O.Caul. 2000. Evidence for airborne transmission of Norwalk-like virus (NLV) in a hotel restaurant. Epidemiol. Infect. 124(3):481–487.

Marlowe, E.M., K.J.Josephson, and I.L.Pepper. 2000. Nucleic acid-based methods of analysis. Pp. 287–318 in Environmental Microbiology, R.M.Maier, I.L.Pepper, and C.P.Gerba, eds. San Diego: Academic Press.

Mbela, K.K. 1988. Evaluation of Temperature Effects on Inactivation of Ascaris Eggs in Both Aerobic and Anaerobic Digestion Processes. M.S. Thesis. Department of Environmental Health Sciences, School of Public Health and Tropical Medicine, Tulane University, New Orleans, LA. May 1988.

McCullough, N.B., and C.W.Eisele. 1951. Experimental human salmonellosis. II. Immunity studies following experimental illness with Salmonella meleagridis and Salmonella anatum. J. Immun. 66(5):595–608.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

McDonell, D.B. 1985. Inactivation of Ascaris Eggs in Municipal Treatment Processes. D.Sc. Dissertation. Department of Environmental Health Sciences, School of Public Health and Tropical Medicine, Tulane University, New Orleans, LA. April 1985.

McGinley, K.J., E.L.Larson, and J.J.Leyden. 1988. Composition and density of microflora in the subungual space of the hand. J. Clin. Microbiol. 26(5):950–953.

McNab, W.B. 1998. A general framework illustrating an approach to quantitative microbial food safety risk assessment. J Food Prot. 61(9):1216–1228.

Medema, G.J., P.F.M.Teunis, A.H.Havelaar, and C.N.Haas. 1996. Assessment of the dose-response relationship of Campylobacter jejuni . Int. J. Food Microbiol. 30(1-2):101-111.

Meehan, P.P., R.S.Reimers, T.G.Akers, M.D.Little, M.C.Metcalf, and C.P.Lo. 1986. Development of Chemical Fixation Process to PFRP Classification for Municipal Sludge Treatment Enabling the Reuse of the Resulting Product. Phase I SBIR Report to U.S. Environmental Protection Agency. April 1986.

Melbostad, E., W.Eduard, A.Skogstad, P.Sanden, J.Lassen, P.Søstrand, and K. Heldal. 1994. Exposure to bacterial aerosols and work-related symptoms in sewage workers. Am. J. Ind. Med. 25(1):59–63.

Michel, O., R.Ginanni, J.Duchateau, F.Vertongen, B.Le Bon, and R.Sergysels. 1991. Domestic endotoxin exposure and clinical severity of asthma. Clin. Exp. Allergy 21(4):441–448.

Michel, O., R.Ginanni, B.Le Bon, J.Content, J.Duchateau, and R.Sergysels. 1992. Inflammatory response to acute inhalation of endotoxin in asthmatic patients. Am. Rev. Respir. Dis. 146(2):352–357.

Michel, O., J.Kips, J.Duchateau, F.Vertongen, L.Robert, H.Collet, R.Pauwels, and R.Sergysels. 1996. Severity of asthma is related to endotoxin in house dust. Am. J. Respir. Crit. Care Med. 154(6 Pt. 1):1641–1646.

Millner, P.D., S.A.Olenchock, E.Epstein, R.Rylander, J.Haines, J.Walker, B.L.Ooi, E.Horne, and M.Maritato. 1994. Biosolids associated with composting facilities. Compost Science and Utilization 2(4):6–57.

Monroe, S.S., T.Ando, and R.I.Glass. 2000. Introduction: Human enteric caliciviruses: An emerging pathogen whose time has come. J. Infect. Dis. 181(Suppl. 2):S249–S251.

Morris, M.C., M.A.Joyce, A.C.Heath, B.Rabel, and G.W.Delisle. 1997. The responses of Lucilla cuprina to odours from sheep, offal, and bacterial cultures. Med. Vet. Entomol. 11(1):58–64.

Morris, R.D., E.N.Naumova, and J.K.Griffiths. 1998. Did Milwaukee experience waterborne cryptosporidiosis before the large documented outbreak in 1993? Epidemiology 9(3):264–270.

Murphy, J.W. 1990. Immunity to fungi. Curr. Opin. Immunol. 2(3):360–367.

Newby, D.T., I.L.Pepper, and R.M.Maier. 2000a. Microbial transport. Pp. 147–175 in Environmental Microbiology, R.Maier, I.L.Pepper, and C.P.Gerba, eds. San Diego: Academic Press.

Newby, D.T., T.J.Gentry, and I.L.Pepper. 2000b. Comparison of 2,4-dichlorophenoxyacetic acid degradation and plasmid transfer in soil resulting

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

from bioaugmentation with two different pJP4 donors. Appl. Environ. Microbiol. 66(8):3399–3407.

Nielsen, B.H., E.M.Nielsen, and N.O.Breum. 2000. Seasonal variation in bioaerosols exposure during biowaste collection and measurements of leaked percolate. Waste Manage. Res. 18(1):64–72.

Nishijima, S., S.Namura, S.Kawai, H.Hosokawa, and Y.Asada. 1995. Staphylococcus aureus on hand surface and nasal carriage in patients with atopic dermatitis. J. Am. Acad. Dermatol. 32(4):677–679.

Noble, W.C. 1998. Skin bacteriology and the role of Staphylococcus aureus in infection. Br. J. Dermatol. 139(Suppl. 53):9–12.

NRC (National Research Council). 1983. Risk Assessment in the Federal Government: Managing the Process. Washington DC: National Academy Press.

NRC (National Research Council). 1989. Drinking Water and Health, Vol. 9. Selected Issues in Risk Assessment. Washington, DC: National Academy Press.

Ochman, H., J.G.Lawrence, and E.A.Groisman. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405(6784):299–304.

Okazaki, M., B.Umeda, M.Koide, and A.Saito. 1998. Legionella longbeachae pneumonia in a gardener, [in Japanese]. Kansenshogaku Zasshi. 72(10):1076–1079.

Okhuysen, P.C., C.L.Chappell, J.H.Crabb, C.R.Sterling, and H.L.DuPont. 1999. Virulence of three distinct Cryptosporidium parvum isolates for healthy adults. J. Infect. Dis. 180(4):1275–1281.

Ongerth, J.E. 1989. Giardia cyst concentrations in river water. Am. Water Works Assoc. J. 81(9):81–86.

Ottolenghi, A.C., and V.V.Hamparian. 1987. Multiyear study of sludge application to farmland: Prevalence of bacterial enteric pathogens and antibody status of farm families. Appl. Environ. Microbiol. 53(5):1118–1124.

Overgaauw, P.A. 1997. Aspects of Toxocara epidemiology: Human toxocarosis. Crit Rev. Microbiol. 23(3):215–231.


Pahren, H.R. 1987. Microorganisms in municipal solid waste and public health implications. CRC Crit. Rev. Environ. Control 17(3):187–228.

Papapetropoulou, M., and A.C.Vantarakis. 1998. Detection of adenovirus outbreak at a municipal swimming pool by nested PCR amplification. J. Infect. 36(1):101– 103.

Pasquill, F. 1962. Atmospheric Diffusion: The Dispersion of Windborne Material from Industrial and Other Sources. London: Van Nostrand.

Patel, K.D. 1996. Enhancement of Anaerobic Digestion Processes Using Pulse Power Technology. M.S. Thesis. Department of Environmental Health Science, School of Public Health, Tulane University, New Orleans, LA. December 1996.

Payment, P., and E.Franco. 1993. Clostridium perfringens and somatic coliphages as indicators of the efficiency of drinking water treatment for viruses and protozoan cysts. Appl. Environ. Microbiol. 59(8):2418–2424.

Peden, D.B., K.Tucker, P.Murphy, L.Newlin-Clapp, B.Boehlecke, M.Hazucha, P. Bromberg, and W.Reed. 1999. Eosinophil influx to the nasal airway after local LPS challenge in humans. J. Allergy Clin. Immunol. 104(2 Pt. 1):388–394.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

Pedgley. D.E. 1991. Aerobiology: The atmosphere as a source and sink for microbes. Pp. 43–59 in Microbial Ecology of Leaves, J.H.Andrews, and S.S. Hirano, eds. New York: Springer-Verlag.

Pena, J., S.C.Ricke, C.L.Shermer, T.Gibbs, and S.D.Pillai. 1999. A gene amplification-hybridization sensor based methodology to rapidly screen aerosol samples for specific bacterial gene sequences. J. Environ. Sci. Health Part A 34(3):529–556.

Pepper, I.L., K.L.Josephson, R.L.Bailey, M.D.Burr, and C.P.Gerba. 1993. Survival of indicator organisms in Sonoran Desert soil amended with sewage sludge. J. Environ. Sci. Health Part A Environ. Sci. Eng. 28(6):1287–1302.

Pickering, L.K., A.V.Bartlett, R.R.Reves, and A.Morrow. 1988. Asymptomatic excretion of rotavirus before and after rotavirus diarrhea in children in day care centers. J. Pediatr. 112(3):361–365.

Pillai, S.D., E.Rubio, and S.C.Ricke. 1996. Prevalence of fluoroquinolone-resistant Escherichia coli in agricultural and municipal waste streams. Bioresourc. Technol. 58(1):57–60.

Pillai, S.D., K.W.Widmer, S.E.Dowd, and S.C.Ricke. 1996. Occurrence of airborne bacteria and pathogen indicators during land application of sewage sludge. Appl. Environ. Microbiol. 62(1):296–299.

Pillai, S.D., K.W.Widmer, K.G.Maciorowski, and S.C.Ricke. 1997. Antibiotic resistance profiles of Escherichia coli isolated from rural and urban environments. J. Environ. Sci. Health. Part A 32(6):1665–1675.

Reed, C.E., and D.K.Milton. 2001. Endotoxin-stimulated innate immunity: A contributing factor for asthma. J. Allergy Clin. Immunol. 108(2):157–166.

Regli, S., J.B.Rose, C.N.Haas, and C.P.Gerba. 1991. Modeling risk from giardia and viruses in drinking water. Am. Water Works Assoc. J. 83(11):76–84.

Reimers, R.S., A.C.Anderson, A.A.Abdelhgani, M.C.Lockwood, and L.E.White. 1986a. The usage of non-ionizing irradiation processes in the disinfection of water and wastes. Pp. 272–299 in Applied Fields for Energy Conservation, Water Treatment, and Industrial Applications, Final Report, R.S.Reimers, S.F.Bock, and L.E.White, eds. DOE/CE/40568-T1 (DE86014306). Washington, DC: Technical Information Center, Office of Scientific and Technical Information, U.S. Dept. of Energy. June 1986.

Reimers, R.S., D.D.Bowman, P.L.Schafer, P.Tata, B.D.Leftwich, and M.M.Atique. 2001. Factors Affecting Lagoon Storage Disinfection of Biosolids. Proceedings of Joint WEF/AWWA/CWEA Specialty Conference “Biosolids 2001”, CD-ROM. Water Environmental Federation, Alexandria, VA. February 2001.

Reimers, R.S., A.J.Englande, R.M.Bakeer, D.D.Bowman, T.A.Calamari, H.B.Bradford, C.F.Dufrechou, and M.M.Atique. 1999. Update on Current and Future Aspects of Resource Management for Animal Wastes. WEFTEC ’99 Pre-Conference Workshop “Beneficial Use of Animal Waste Residuals—A Mandatory Aim for the 21st Century.” Water Environment Federation, Alexandria, VA. October 1999.

Reimers, R.S., M.D.Little, T.G.Akers, W.D.Henriques, D.B.McDonell, and K.K. Mbela. 1990. Persistance of pathogens in lagoon-stored sludge. EPA 600/S2-

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

89/815. Risk Reduction Engineering Laboratory, U.S. Environmental Protection Agency, Research Triangle Park, NC. January, 1990.

Reimers, R.S., M.D.Little, A.J.Englande, D.B.Leftwich, D.D.Bowman, and R.F. Wilkinson. 1981. Parasites in Southern Sludges and Disinfection by Standard Sludge Treatment. EPA 600/2–81–166. NTIS PB 82–102344. Prepared by the School of Public Health and Tropical Medicine, Tulane University, New Orleans, LA, for the Municipal Environmental Research Laboratory, Cincinnati, OH.

Reimers, R.S., M.D.Little, A.J.Englande, D.B.McDonell, D.D.Bowman, and J.M. Hughes. 1986b. Investigation of Parasites in Sludges and Disinfection Techniques. EPA 600/1–85/022. NTIS PB 86–135407. Prepared by the School of Public Health and Tropical Medicine, Tulane University, New Orleans, LA, for the Health Effects Research Laboratory, Research Triangle Park, NC.

Reimers, R.S., M.D.Little, A.Lopez, and K.K.Mbela. 1991. Final Testing of the Synox Municipal Sludge Treatment for PFRP Approval—Phase II. Report to Synox Corporation, Bethesda, MD, by School of Public Health and Tropical Medicine, Tulane University, New Orleans, LA. December 4, 1991.

Reimers, R.S., D.B.McDonell, M.D.Little, T.G.Akers, and W.D.Henriques. 1985. Chemical Inactivation of pathogens in municipal sludges. In Control of Sludge Pathogens, Series IV, WPCF Pre-Conference Workshop on “Municipal Wastewater Sludge Disinfection,” Kansas City, MO, October 1985. Washington, DC: Water Pollution Control Federation.

Reynolds, K.A., C.P.Gerba, and I.L.Pepper. 1996. Detection of infectious enteroviruses by an integrated cell culture-PCR procedure. Appl. Environ. Microbiol. 62(4):1424–1427.

Reynolds, K.A., C.P.Gerba, and I.L.Pepper. 1997. Rapid PCR-based monitoring of infectious enteroviruses in drinking water. Water Sci. Techol. 35(11–12):423–427.

Rice, E.W. 1999. Escherichia coli. Pp. 75–78 in Waterborne Pathogens, 1st Ed. AWWA Manual M48. Denver, CO: American Water Works Association.

Ritter, W.F., J.G.McDermott, A.E.M.Chirnside, and R.W.Scarborough. 1992. Land application of lime stabilized septage. J. Environ. Sci. Health Part A Environ. Sci. Eng. 27(7):1701–1720.

Rohwer, R.G. 1984. Scrapie infectious agent is virus-like in size and susceptibility to inactivation. Nature 308(5960):658–662.

Rose, J.B. 1990. Sampling and analytical methods. Environmental sampling for waterborne pathogens: Overview of methods, application limitations and data interpretation. Pp. 223–234 in Methods for the Investigation and Prevention of Waterborne Disease Outbreaks, G.F.Craun, ed. EPA/600/1–90/005a. Health Effects Research Laboratory, U.S. Environmental Protection Agency, Cincinnati, OH.

Rose, J.B., C.P.Gerba, and W.Jakubowski. 1991a. Survey of potable water supplies for Cryptosporidium and Giardia. Environ. Sci. Technol. 25(8):1393–1400.

Rose, J.B., C.N.Haas, and S.Regli. 1991b. Risk assessment and the control of waterborne giardiasis. Am. J. Public Health 81(6):709–713.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

Sabalos, C.M. 1998. Detection of Enteric Viruses in Treated Wastewater Sludge Using Cell Culture and Molecular Methods. M.S. Thesis. University of Arizona, Tucson, AZ. August 1998.

Saiki, R.K., D.H.Gelfand, S.Stoffel, S.J.Scharf, R.Higuchi, G.T.Horn, K.B.Mullis, and H.A.Erlich. 1988. Primer directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239(4839):487–491.

Schiffman, S.S., J.M.Walker, P.Dalton, T.S.Lorig, J.H.Raymer, D.Shusterman, and C.M.Williams. 2000. Potential health effects of odor from animal operations, wastewater treatment, and recycling of byproducts. J. Agromed. 7(1):7–81.

Schijven, J.F. 2001. Virus Removal from Groundwater by Soil Passage. Modeling, Field and Laboratory Experiments. Ph.D. Dissertation. Technische Universiteit, Delft, The Netherlands.

Schijven, J.F., and L.C.Rietveld. 1996. How do field observations compare with models of microbial removal? The Groundwater Foundation 12th Annual Fall Symposium “Under the Microscope: Examining Microbes in Groundwater,” Boston, September 1996.

Silbergeld, E.K. 1993. Risk assessment: The perspective and experience of U.S. environmentalists. Environ. Health Perspect 101(2):100–104.

Soares, H.M., B.Cardenas, D.Weir, and M.S.Switzenbaum. 1995. Evaluating pathogen regrowth in biosolids compost. Biocycle 36(6):70–76.

Sobsey, M.D. 1978. Field survey of enteric viruses in solid waste landfill leachates. Am. J. Public Health 68(9):858–864.

Sobsey, M.D., C.Wallis, and J.L.Melnick. 1975. Studies on the survival and fate of enteroviruses in an experimental model of a municipal solid waste landfill and leachate. Appl. Microbiol. 30(4):565–574.

Sobsey, M.D., R.M.Hall, and A.E.Burrus. 1991. Evaluation of the SYNOX Process for Disinfection of Raw Municipal Wastewater Sludge. Report to SYNOX Corporation, by Department of Environmental Sciences and Engineering, School of Public Health, University of North Carolina. December 1991.

Sorber, C.A., B.E.Moore, D.E.Johnson, H.J.Harding, and R.E.Thomas. 1984. Microbiological aerosols from the application of liquid sludge to land. J. Water Pollut Control Fed. 56(7):830–836.

Sorvillo, F., L.R.Ash, O.G.Berlin, and S.A.Morse. 2002. Baylisascaris procyonis: An emerging helminthic zoonosis. Emerg. Infect. Dis. 8(4):355–359.

Southworth, R.M. 2001. The U.S. EPA Part 503 Pathogen and Vector Attraction Reduction Requirements. U.S. Environmental Protection Agency.

Spicer, R.C., and H.J.Gangloff. 2000. Limitations in application of Spearman’s rank correlation to bioaerosols sampling data. AIHAJ 61(3):362–366.

Stampi, S., F.Zanetti, A.Crestani, and G.De Luca. 2000. Occurrence and seasonal variation of airborne gram negative bacteria in a sewage treatment plant. New Microbiol. 23(1):97–104.

Straub, T.M., I.L.Pepper, and C.P.Gerba. 1992. Persistence of viruses in desert soils amended with anaerobically digested sewage sludge. Appl. Environ. Microbiol. 58(2):636–641.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

Straub, T.M., I.L.Pepper, and C.P.Gerba. 1993a. Virus survival in sewage sludge amended desert soil. Water Sci. Technol. 27(3/4):421–424.

Straub, T.M., I.L.Pepper, and C.P.Gerba. 1993b. Hazards from pathogenic microorganisms in land-disposed sewage sludge. Rev. Environ. Contain. Toxicol. 132:55–91.

Straub, T.M., I.L.Pepper, and C.P.Gerba. 1995. Comparison of PCR and cell culture for detection of enteroviruses in sludge-amended field soils and determination of their transport. Appl. Environ. Microbiol. 61(5):2066–2068.

Taylor, D.M., K.Fernie, I.McConnell, and P.J.Steele. 1999. Survival of scrapie agent after exposure to sodium dodecyl sulphate and heat. Vet. Microbiol. 67(1):13-16.

Taylor, D.S., C.D.Richmond, and J.B.Hunt. 1999. Cultural control of larval mosquito production in a fallow citrus grove used for disposal of secondary-treated sewage effluent. J. Am. Mosq. Control Assoc. 15(1):65–68.

Taylor, M.R. 2001. The epidemiology of ocular toxocariasis. J. Helminthol. 75(2):109–118.

Terzieva, S., J.Donnelly, V.Ulevicius, S.A.Grinshpun, K.Willeke, G.N.Stelma, and K.P.

Brenner. 1996. Comparison of methods for detection and enumeration of airborne microorganisms collected by liquid impingement. Appl. Environ. Microbiol. 62(7):2264–2272.

Teunis, P.F., N.J.Nagelkerke, and C.N.Haas. 1999. Dose response models for infectious gastroenteritis. Risk Anal. 19(6):1251–1260.

Thorne, P.S. 2000. Inhalation toxicology models of endotoxin- and bioaerosol-induced inflammation. Toxicology 152(1–3):13–23.


Van Ryzin, J. 1980. Quantitative risk assessment J. Occup. Med. 22(5):321–326.

Van Tongeren, M., L.Van Amelsvoort, and D.Heederick. 1997. Exposure to organic dusts, endotoxins, and microorganisms in the municipal waste industry. Int. J. Occup. Environ. Health 3(1):30–36.

Venosa, A.D. 1985. Detection and Significance of Pathogens in Sludges. In Control of Sludge Pathogens, Series IV, WPCF Pre-Conference Workshop on “Municipal Wastewater Sludge Disinfection,” Kansas City, MO, October 1985. Washington, DC: Water Pollution Control Federation.

Voss, J.G. 1975. Effects of an antibacterial soap on the ecology of aerobic bacterial flora of human skin. Appl. Microbiol. 30(4)551–556.


Ward, R.L., G.A.McFeters, and J.G.Yeager. 1984. Pathogens in Sludge: Occurrence, Inactivation, and Potential Regrowth. SAND83–0557. Albuquerque, NM: Sandia National Laboratories. 78pp. July 1984.

Watkins, J., and K.P.Sleath. 1981. Isolation and enumeration of Listeria monocytogenes from sewage, sewage sludge, and river water. J. Appl. Bacteriol. 50(1):1–9.

Wei, S., P.Walsh, R.Huang, and S.S.To. 2000. 93G, a novel sporadic strain of hepatitis E virus in South China isolated by cell culture. J. Med. Virol. 61(3):311– 318.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×

Welbourn, E, R.H.Champion, and W.E.Parish. 1976. Hypersensitivity to bacteria in eczema. I. Bacterial culture, skin tests and immunofluorescent detection of immunoglobulins and bacterial antigens. Br. J. Dermatol. 94(6):619–632.

White, K.E., M.T.Osterbolm, J.A.Mariotti, J.A.Korlath, D.H.Lawrence, T.L. Ristinen, and H.B.Greenberg. 1986. A foodborne outbreak of Norwalk virus gastroenteritis. Evidence for post-recovery transmission. Am. J. Epidemiol. 124(1):120–126.

Wickman, H.H. 1994. Deposition, adhesion and release of bioaerosol. Pp. 99–165 in Atmospheric Microbial Aerosols, Theory and Applications, B.Lighthart, and A.J.Mohr, eds. New York: Chapman & Hall.

Wolk, D.M., C.H.Johnson, E.W.Rice, M.M.Marshall, K.F.Grahn, C.B.Plummer, and C.R.Sterling. 2000. A spore counting method and cell culture model for chlorine disinfection studies of Encephalitozoon syn. Septata intestinalis. Appl. Environ. Microbiol. 66(4):1266–1273.

Yang, Y.C. 1996. Abiotic Factors in Biosolids Processing that Influence Pathogen Disinfection (Nitrous Acids and Ammonia Studies). M.S. Thesis. School of Public Health and Tropical Medicine, Tulane University, New Orleans, LA. June 1996.

Yanko, W.A 1987. Occurrence of Pathogens in Distribution and Marketing Municipal Sludges. EPA/600/1–87/014. NTIS PB88–15273/AS. Health Effects Research Laboratory, U.S. Environmental protection Agency, Research Triangle Park, NC.

Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 257
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 258
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 259
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 260
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 261
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 262
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 263
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 264
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 265
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 266
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 267
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 268
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 269
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 270
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 271
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 272
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 273
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 274
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 275
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 276
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 277
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 278
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 279
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 280
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 281
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 282
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 283
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 284
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 285
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 286
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 287
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 288
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 289
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 290
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 291
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 292
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 293
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 294
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 295
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 296
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 297
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 298
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 299
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 300
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 301
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 302
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 303
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 304
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 305
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 306
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 307
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 308
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 309
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 310
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 311
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 312
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 313
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 314
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 315
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 316
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 317
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 318
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 319
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 320
Suggested Citation:"6 Evaluation of EPA's Approach to Setting Pathogen Standards." National Research Council. 2002. Biosolids Applied to Land: Advancing Standards and Practices. Washington, DC: The National Academies Press. doi: 10.17226/10426.
×
Page 321
Next: 7 Integration of Chemical and Pathogen Risk Assessment »
Biosolids Applied to Land: Advancing Standards and Practices Get This Book
×
Buy Paperback | $60.00 Buy Ebook | $48.99
MyNAP members save 10% online.
Login or Register to save!
Download Free PDF

The 1993 regulation (Part 503 Rule) governing the land application of biosolids was established to protect public health and the environment from reasonably anticipated adverse effects. Included in the regulation are chemical pollutant limits, operational standards designed to reduce pathogens and the attraction of disease vectors, and management practices. This report from the Board on Environmental Studies and Toxicology evaluates the technical methods and approaches used by EPA to establish those standards and practices, focusing specifically on human health protection. The report examines improvements in risk-assessment practices and advances in the scientific database since promulgation of the regulation, and makes recommendations for addressing public health concerns, uncertainties, and data gaps about the technical basis of the biosolids standards.

  1. ×

    Welcome to OpenBook!

    You're looking at OpenBook, NAP.edu's online reading room since 1999. Based on feedback from you, our users, we've made some improvements that make it easier than ever to read thousands of publications on our website.

    Do you want to take a quick tour of the OpenBook's features?

    No Thanks Take a Tour »
  2. ×

    Show this book's table of contents, where you can jump to any chapter by name.

    « Back Next »
  3. ×

    ...or use these buttons to go back to the previous chapter or skip to the next one.

    « Back Next »
  4. ×

    Jump up to the previous page or down to the next one. Also, you can type in a page number and press Enter to go directly to that page in the book.

    « Back Next »
  5. ×

    Switch between the Original Pages, where you can read the report as it appeared in print, and Text Pages for the web version, where you can highlight and search the text.

    « Back Next »
  6. ×

    To search the entire text of this book, type in your search term here and press Enter.

    « Back Next »
  7. ×

    Share a link to this book page on your preferred social network or via email.

    « Back Next »
  8. ×

    View our suggested citation for this chapter.

    « Back Next »
  9. ×

    Ready to take your reading offline? Click here to buy this book in print or download it as a free PDF, if available.

    « Back Next »
Stay Connected!