Conference Paper

Comparative Microbial Risks of Land Applied Biosolids and Animal Manure

Authors:
To read the full-text of this research, you can request a copy directly from the authors.

Abstract

The transmission of pathogens by land application of untreated human and animal wastes has been known for more than 100 years. In the United States there are more than 450,000 (EPA) animal feeding operations producing more than 100 times as much manure as sewage sludge produced by municipal wastewater treatment plants. In addition, grazing animals also deposit large quantities of manure on range land. This study attempts to look at the relative risks of pathogens in biosolids vs. animal manure (feces) applied to land using a quantitative microbial risk assessment approach. This process involves four basic steps: pathogen identification, exposure assessment, dose-response and risk characterization. Several examples which were evaluated included: risk to workers, consumption of produce crops, and children playing in a field. While some of these exposures are less likely for biosolids applications because of site and application restrictions, they can commonly occur in areas where manure is applied. The risks are largely determined by the degree of treatment that the manure receives before land application, and risks compared to biosolids are often greater or comparable, depending upon assumptions used in the risk model. Generally, annual risks of infection were greater than the 1:10,000 chance of infection for bacteria (manures) and viruses (biosolids) when land applied and assuming an 1 month decay time period. Using more appropriate conditions of pathogen die-off in the soil (> 6 months), land application of either residual resulted in risks less than 1:10,000 per year. Assuming USDA-AMS and USEPA recommended guidelines and regulations are followed for crops grown on waste-applied land, risks associated with manure or biosolids land application are well below the 1:10,000 per year risk of infection standard. This analysis provides insight on the relative risks of animal waste and biosolid land application that allows for a better understanding of the risks to the general public and the industry.

No full-text available

Request Full-text Paper PDF

To read the full-text of this research,
you can request a copy directly from the authors.

... Note that the study by Viau et al (2011) is not included in Table 2 as it is a literature review. Further, the study by Brooks et al (2009) was not considered due to its partial overlap with the study by Brooks et al (2012). Table 1 Overview of the focus of previous QMRA studies. ...
... Assessment of occupational risks to humans from aerosolisation of microorganisms from biosolids. Brooks et al (2009) Land application of sewage sludge and manure. Comparison of the microbial risks to humans of land applied sewage sludge and animal manure. ...
... Many earlier QMRA studies assessing pathogen risk related to municipal wastewater and sewage sludge management 6,[11][12][13][14][15][16][17][18][19] calculated the probability of infection (or illness) per individual and event, or per individual and year, or the number of cases of infection (or illness) for each combination of pathogen and exposure pathway included in the respective study. These earlier studies did not address how the risks resulting from various pathogens and exposure pathways can be aggregated to a cumulative pathogen risk, and how this pathogen risk compares with other potential impacts on human health. ...
... This study was based on eight previous QMRA studies [11][12][13][14][16][17][18][19] on pathogen risk related to municipal wastewater and sewage sludge management. More details on these studies are provided in the Supporting Information (e.g., focus of the respective study, pathogens and exposure pathways covered, assessment endpoints applied). ...
Article
Full-text available
The environmental performance of wastewater and sewage sludge management is commonly assessed using life cycle assessment (LCA), whereas pathogen risk is evaluated with quantitative microbial risk assessment (QMRA). This study explored the application of QMRA methodology with intent to include pathogen risk in LCA and facilitate a comparison with other potential impacts on human health considered in LCA. Pathogen risk was estimated for a model wastewater treatment system (WWTS) located in an industrialized country and consisting of primary, secondary and tertiary wastewater treatment, anaerobic sludge digestion, and land application of sewage sludge. The estimation was based on eight previous QMRA studies as well as parameter values taken from the literature. A total pathogen risk (expressed as burden of disease) in the order of 0.2 - 9 disability-adjusted life years (DALY) per year of operation was estimated for the model WWTS serving 28,600 persons, and for the pathogens and exposure pathways included in this study. The comparison of pathogen risk with other potential impacts on human health considered in LCA is detailed in part 2 of this article series.
... Recent studies have attempted to quantify occupational and public microbial risks associated with land-applied biosolids (Dowd et al., 2000;Eisenberg et al., 2004Eisenberg et al., , 2008Gale, 2005;Brooks et al., 2005Brooks et al., , 2009bTanner et al., 2008;Viau et al., 2011). Risks have ranged from low (<10 −12 per year) to as high as 1 (100%), for "worst-case" conditions (e.g., minimal personal protective equipment, high pathogen load, high wind speed). ...
... One such approach is to use a wide range of reported values including the lower and upper pathogen levels, essentially encompassing the range of mean pathogen levels expected for a given source. Th is approach has been applied in residual risk analyses by Brooks et al. (2005Brooks et al. ( , 2009b, Tanner et al. (2008), ASM (2011), and the current study. A Monte Carlo analysis would accomplish this as well (Viau et al., 2011). ...
Article
Land application is a practical use of municipal Class B biosolids and manure that also promotes soil fertility and productivity. To date, no study exists comparing biosolids to manure microbial risks. This study used quantitative microbial risk assessment to estimate pathogen risks from occupational and public exposures during scenarios involving fomite, soil, crop, and aerosol exposures. Greatest one-time risks were from direct consumption of contaminated soil or exposure to fomites, with one-time risks greater than 10. Recent contamination and high exposures doses increased most risks. and enteric viruses provided the greatest single risks for most scenarios, particularly in the short term. All pathogen risks were decreased with time, 1 d to14 mo between land application and exposure; decreases in risk were typically over six orders of magnitude beyond 30 d. Nearly all risks were reduced to below 10 when using a 4-mo harvest delay for crop consumption. Occupational, more direct risks were greater than indirect public risks, which often occur after time and dilution have reduced pathogen loads to tolerable levels. Comparison of risks by pathogen group confirmed greater bacterial risks from manure, whereas viral risks were exclusive to biosolids. A direct comparison of the two residual types showed that biosolids use had greater risk because of the high infectivity of viruses, whereas the presence of environmentally recalcitrant pathogens such as and maintained manure risk. Direct comparisons of shared pathogens resulted in greater manure risks. Overall, it appears that in the short term, risks were high for both types of residuals, but given treatment, attenuation, and dilution, risks can be reduced to near-insignificant levels. That being said, limited data sets, dose exposures, site-specific inactivation rates, pathogen spikes, environmental change, regrowth, and wildlife will increase risk and uncertainty and remain areas poorly understood.
Article
Despite the global push for a circular water and nutrient economy, the United States still lags in recycling and reusing valuable waste streams. The reuse of waste streams could result in more sustainable agricultural practices by reducing water withdrawals in stressed environments and nutrient inputs to eutrophication-impacted ecosystems. However, microbial risks are a key barrier to reuse. We identify research and regulatory gaps through a systematic review of quantitative microbial risk assessments (QMRAs) and regulations for biosolids, manure, and human source-separated urine. We propose a cohesive path forward to improve upon existing QMRA approaches, to combine QMRA with other risk frameworks, and to develop integrated monitoring and control strategies by incorporating molecular biology tools. The application of a farm-to-fork risk-based approach that considers the combined use of waste streams is needed to develop comprehensive best management practices, treatment recommendations, and microbial quality criteria that promote food safety while advancing agricultural sustainability.
Article
Full-text available
This study evaluates the occurrence of Cryptosporidium oocysts and Giardia cysts in reclaimed effluents if method 1623 with the Envirochek capsule filters (standard and high-volume [HV] filters) and a modified version of the Information Collection Rule method (ICR) with the polypropylene yarn-wound cartridge filter are used. The recovery efficiency of the analytical methods was evaluated with samples of reagent, tap, and reclaimed water by using flow cytometer-sorted spike suspensions. (Oo)cyst recovery efficiency determined filter performance and method reproducibility in the water matrix tested. Method 1623 with the Envirochek HV capsule filter generated significantly higher recovery rates than did the standard Envirochek filter and the modified ICR method. Notwithstanding, large variations in recovery rates (>80%) occurred with samples of reclaimed water, and none of the water quality parameters analyzed in the reclaimed effluents could explain such variability. The highest concentrations of indigenous oocysts were detected by method 1623 with the HV filter, which provided a sufficient number of oocysts for further confirmation of infectious potential. Confirmation of species and potential infectivity for all positive protozoan samples was made by using a nested PCR restriction fragment polymorphism assay and the focus detection method most-probable-number assay, respectively. The methodology and results described in the present investigation provide useful information for the establishment of pathogen numeric standards for reclaimed effluents used for unrestricted irrigation.
Article
Monitoring data and dose-response models were used to evaluate risks associated with viruses and protozoa at a full-scale reclamation facility. Indigenous indicator and pathogenic microorganisms were monitored at different stages of treatment for 1 yr at a full-scale water reclamation facility that produced reclaimed water for residential irrigation. The combination of biological treatment, sand filtration, and chlorination employed at the plant reduced total and fecal coliforms by > 7 log10 and coliphages and enteroviruses by > 5 log10. Protozoa (Cryptosporidium and Giardia spp.) were reduced by > 3 log10. Viruses and protozoa were detected in the reclaimed water at levels between 0.01 and 5 per 100 l. The addition of large numbers of bacteriophage as a tracer permitted an assessment of inactivation and/or removal by the filtration and chlorination units, which were shown to provide 1.6 and 1.5 log10 reductions, respectively. Analysis of the risk associated with exposure to the reclaimed water shows that the probability of infection following a single exposure to 100 ml of the water was between 10−6 (1 in a million) and 10−8 (1 in 100 million) for landscape irrigation. In general, anaerobic treatment of residual solids produced during the wastewater treatment process reduced the levels of indicator and pathogenic microorganisms by approximately 1 log10. The levels of viruses detected in the final residual would not meet acceptable levels for land application for class A residuals according to EPA regulations.
Article
The World Health Organization and others have proposed international guidelines for the safe reuse of domestic wastewater. Treatment and microbial standards have been suggested with varying microbial water quality targets to suit local circumstances of affordability and health risks. However, it is important to recognize that universal application of bacterial standards for water quality assessment will not yield the same risks from microbial pathogens in reclaimed wastewater around the world. The concentration and types of pathogens in raw wastewater varies from one region of the world to another depending on the incidence in the community. This is influenced by the general hygiene, season, and per capita water use. Also, different treatment processes may be more effective in removing indicator bacteria and certain groups of pathogens than others. Proposed guidelines have also neglected the importance of water in the transmission of viral and bacterial diseases in developed countries and their impact on morbidity and mortality. Additional research is needed to better reduce the uncertainly of proposed guidelines for water recycling and to better define the risks associated to the exposed populations.
Article
A risk assessment approach was used to estimate the public health impacts from exposure to human rotavirus in drinking and recreational waters. Rotavirus is the major cause of viral gastroenteritis worldwide and several waterborne outbreaks have been documented. This results in a significant economic impact on society in terms of direct medical costs, loss of work, quality of life and mortality. The virus is common in domestic wastewater and polluted surface waters. Dose-response data in human adult volunteers indicate that it is the most infective of all the enteric viruses, and this was used to develop a microbial risk assessment model to estimate daily and yearly risks of infection, morbidity and mortality for exposure via drinking and recreational waters using existing information on the occurrence of rotavirus. The disease is most severe for the very young, the elderly, and the immunocompromised. Case fatality rates in the United States are 0.01% in the general population, 1% in the elderly, and up to 50% in the immunocompromised. Analysis indicates that significant risks of disease (5 × 10−1−2.45 × 10−3) could result for drinking and recreational waters in which rotavirus has been detected. The major limitation in assessing the risks of waterborne rotaviral infections at present is the lack of data on its occurrence in water and the potential for human exposure.
Article
The doses of UV irradiation necessary to inactivate selected enteric viruses on the U.S. Environmental Protection Agency Contaminant Candidate List were determined. Three-log reductions of echovirus 1, echovirus 11, coxsackievirus B3, coxsackievirus B5, poliovirus 1, and human adenovirus type 2 were effected by doses of 25, 20.5, 24.5, 27, 23, and 119 mW/cm2, respectively. Human adenovirus type 2 is the most UV light-resistant enteric virus reported to date.
Article
Among ten patients who contracted sporadic acute or fulminant hepatitis E between 2001 and 2002 in Hokkaido, Japan, nine (90 %) had a history of consuming grilled or undercooked pig liver 2-8 weeks before the disease onset. We tested packages of raw pig liver sold in grocery stores as food in Hokkaido for the presence of hepatitis E virus (HEV) RNA by RT-PCR. Pig liver specimens from seven (1.9 %) of 363 packages had detectable HEV RNA. Partial sequence analyses revealed that the seven swine HEV isolates belonged to genotype III or IV. One swine HEV isolate (swJL145) from a packaged pig liver had 100 % identity with the HE-JA18 isolate recovered from an 86-year-old patient in Hokkaido. Two swine HEV isolates (swJL234 and swJL325) had 98.5-100 % identity with the HE-JA4 isolate obtained from a 44-year-old patient in Hokkaido. These results indicate that inadequately cooked pig liver may transmit HEV to humans.
Article
There is increasing interest in the development of a microbial risk assessment methodology for regulatory and operational decision making. This document presents a methodology for assessing risks to human health from pathogen exposure using a population-based model that explicitly accounts for properties unique to an infectious disease process, specifically secondary transmission and immunity. To demonstrate the applicability of this risk-based method, numerical simulations were carried out for a case study example in which the route of exposure was direct consumption of biosolids-amended soil and the pathogen present in the soil was enterovirus. The output from the case study yielded a decision tree that differentiates between conditions in which the relative risk from biosolids exposure is high and those conditions in which the relative risk from biosolids is low. This decision tree illustrates the interaction among the important factors in quantifying risk. For the case study example, these factors include biosolids treatment processes, the pathogen shedding rate of infectious individuals, secondary transmission, and immunity. Further refinement in methods for determining biosolids exposures under field conditions would certainly increase the utility of these approaches.
Article
To determine the prevalence and levels of zoonotic agents in livestock wastes. A proportionally weighted survey was undertaken and livestock waste samples analysed quantitatively for Escherichia coli O157, pathogenic Listeria, Salmonella, Campylobacter, Giardia and Cryptosporidium. A significant proportion of wastes contained at least one zoonotic agent. Relationships were found between dry matter content and the presence and levels of some zoonotic agents. British livestock wastes contain measurable levels of the zoonotic agents that cause most cases of gastroenteritis in the UK. Animal wastes are disposed of by spreading to agricultural land used for the production of crops and livestock grazing. As British wastes are contaminated with significant levels of zoonotic agents, the practice may represent a way for pathogens to travel further up the food chain.
Modeling the final rules. 40 CFR Part 503 Subpart D
  • S Regli
  • J B Rose
  • C N Haas
  • C P Gerba
Regli, S., J.B. Rose, C.N. Haas, and C.P. Gerba. 1991. Modeling the final rules. 40 CFR Part 503 Subpart D. Fed. Regist. 58:9398-9400.
This is due to a number of factors includ Sensitive populations: ing (i) changes in the way we produce our food supply
  • C P -Gerba
  • J B Rose
  • C N Haas
nization, 2003). This is due to a number of factors includ- Gerba, C.P., J.B. Rose, and C.N. Haas. 1996a. Sensitive populations: ing (i) changes in the way we produce our food supply;
Waterstandardized , resulting in better performance. Thus, the borne adenovirus: A risk assessment concentration of pathogens in treated biosolids may be Crook Water reclamation and reuse criteria Wastewater reclamation and reuse Methods for the
  • K D Crabtree
  • C P Gerba
  • J B Rose
  • C N Haas
tions have been in effect, treatment has become more Crabtree, K.D., C.P. Gerba, J.B. Rose, and C.N. Haas. 1997. Waterstandardized, resulting in better performance. Thus, the borne adenovirus: A risk assessment. Water Sci. Technol. 35:1–6. concentration of pathogens in treated biosolids may be Crook, J. 1998. Water reclamation and reuse criteria. p. 627–703. In T. less than 12 to 15 yr ago when the last surveys where Asano (ed.) Wastewater reclamation and reuse. Technomic Publ., Lancaster, PA. conducted (Straub et al., 1993). Methods for the
Microbiological aerosols from the application of World Health Organization Health guidelines for the use of wastewater in agriculture and aquaculture. Report of a WHO scienliquid sludge to land
  • C A Sorber
  • B E Moore
  • D E Johnson
  • H J Harding
  • R F Thomas
Sorber, C.A., B.E. Moore, D.E. Johnson, H.J. Harding, and R.F. Thomas. 1984. Microbiological aerosols from the application of World Health Organization. 1989. Health guidelines for the use of wastewater in agriculture and aquaculture. Report of a WHO scienliquid sludge to land. J. Water Pollut. Control Fed. 56:830–836.
Biological aerosol Gerba et al. (2002a) used a risk assessment approach emission, fate, and transport from municipal and animal wastes. and data for an anaerobically digested sludge to estimate
  • J P Brooks
  • C P Gerba
  • I L Pepper
Brooks, J.P., C.P. Gerba, and I.L. Pepper. 2004. Biological aerosol Gerba et al. (2002a) used a risk assessment approach emission, fate, and transport from municipal and animal wastes. and data for an anaerobically digested sludge to estimate J. Residuals Sci. Technol. 1:15–18.
Administrative Code 15A NCAC 2H 0200. Waste not discharged to surface waters. Dep. of Environ., and its emergence in non-endemic areas
  • H H Worm
  • G Schlauder
  • G Brandstatter
Worm, H.H., G. Schlauder, and G. Brandstatter. 2002. Hepatitis E State of North Carolina. 1996. Administrative Code 15A NCAC 2H 0200. Waste not discharged to surface waters. Dep. of Environ., and its emergence in non-endemic areas. Wien. Klin. Wochenschr. 114:663-670.
National Water Quality Inventory report to Congress. risk from Giardia and viruses in drinking water
USEPA. 1996a. National Water Quality Inventory report to Congress. risk from Giardia and viruses in drinking water. J. Am. Water Works Assoc. 83:76-84. 305b rep. EPA 841-R-97-008. USEPA, Washington, DC.
Water quality: Guidelines, standards and health
  • In The
  • L Fewtrell
  • J Bartram
IN THE ENVIRONMENT Fewtrell, L., and J. Bartram. 2001. Water quality: Guidelines, standards and health. IWA Publ., London.
Quantitative microbial which allow us to identify new pathogens and trace their risk assessment source; (iv) the evolution of pathogens
  • C N Haas
  • J B Rose
  • C P Gerba
Haas, C.N., J.B. Rose, and C.P. Gerba. 1999. Quantitative microbial which allow us to identify new pathogens and trace their risk assessment. John Wiley & Sons, New York. source; (iv) the evolution of pathogens; (v) changing
A risk assesscade , at least one new pathogen per year that could be ment of emerging pathogens of concern in the land application of transmitted through the environment has been recogbiosolids
  • C P Gerba
  • I L Pepper
  • L F Whitehead
Gerba, C.P., I.L. Pepper, and L.F. Whitehead III. 2002b. A risk assesscade, at least one new pathogen per year that could be ment of emerging pathogens of concern in the land application of transmitted through the environment has been recogbiosolids. Water Sci. Technol. 46:225–230.
mune-compromised individuals who have a greater risk Herwaldt Outbreak of cyclosporiasis with imported raspberries Philadelphia, Pennsylvania– of serious illness are increasing in number); and (vi) 788. application of microbial risk assessment to quantify risks
  • A J Da Silva
  • J M Roberts
  • P A Orlandi
  • C C Johnson
A.J. da Silva, J.M. Roberts, P.A. Orlandi, C.C. Johnson, and B.L. mune-compromised individuals who have a greater risk Herwaldt. 2002. Outbreak of cyclosporiasis with imported raspberries Philadelphia, Pennsylvania, 2000. Emerg. Infect. Dis. 8:783– of serious illness are increasing in number); and (vi) 788. application of microbial risk assessment to quantify risks Hutchison, M.L., L.D. Walters, S.M. Avery, B.A. Synge, and A. from environmentally transmitted pathogens.
National engineering handbook: Agricultural waste management field handbook Assessment of methods for detection of infectious Cryptosporidium oocysts and Giardia cysts in reclaimed effluents. ters 4 and 11
  • W Quintero-Betancourt
  • A L Gennaccaro
  • T M Scott
  • J B Usda
Quintero-Betancourt, W., A.L. Gennaccaro, T.M. Scott, and J.B. USDA. 1992. National engineering handbook: Agricultural waste management field handbook. Part 651 (210-AWMFH, 4/92). Chap- Rose. 2003. Assessment of methods for detection of infectious Cryptosporidium oocysts and Giardia cysts in reclaimed effluents. ters 4 and 11. USDA, Washington, DC.
Health, needed. Since the 40 CFR 503 (USEPA, 1993) regulasafety , and environmental concerns of farm animal waste
  • D J Cole
  • V R Hill
  • F J Humenik
  • M D Sobsey
in the different types of wastes after treatment are also Cole, D.J., V.R. Hill, F.J. Humenik, and M.D. Sobsey. 1999. Health, needed. Since the 40 CFR 503 (USEPA, 1993) regulasafety, and environmental concerns of farm animal waste. Occup. Med. 14:423–448.
Pathogen standards for re- www/housing
  • D York
  • L Walker-Coleman
York, D., and L. Walker-Coleman. 2000. Pathogen standards for re- www/housing/ahs/03dtchrt/tab2-1.html (verified 11 Nov. 2004).
Environmental impacts of animal feeding operations
  • Usepa
  • J Wash-Santamaria
  • G A Toranzos
USEPA. 1998. Environmental impacts of animal feeding operations. USEPA Office of Water, Standards and Applied Sci. Div., Wash-Santamaria, J., and G.A. Toranzos. 2003. Enteric pathogens and soil: A short review. Int. Microbiol. 6:5-9. ington, DC.
Effect of soil or inhalation rates, and duration of exposure during properties on saturated and unsaturated virus transport through these activities. Data on the concentrations of pathogens columns
  • Y Chu
  • Y Jin
  • T Baumann
  • M V Yates
Chu, Y., Y. Jin, T. Baumann, and M.V. Yates. 2003. Effect of soil or inhalation rates, and duration of exposure during properties on saturated and unsaturated virus transport through these activities. Data on the concentrations of pathogens columns. J. Environ. Qual. 32:2017–2025.
Clean water needs survey report to Congress. EPA 832-R-003. USEPA, Washington, DC. criteria for foods with quantitative risk assessment
  • J B Rose
  • C N Haas
  • C P Gerba
Rose, J.B., C.N. Haas, and C.P. Gerba. 1995. Linking microbiological USEPA. 1997. 1996 Clean water needs survey report to Congress. EPA 832-R-003. USEPA, Washington, DC. criteria for foods with quantitative risk assessment. J. Food Saf. 15: 121-132.
Assessment and management USEPA Development document for the proposed revisions to the national pollutant discharge elimination system regulation and of watershed microbial contaminants
  • J E Smith
  • J M Jr
  • Perdek
Smith, J.E., Jr., and J.M. Perdek. 2003. Assessment and management USEPA. 2001. Development document for the proposed revisions to the national pollutant discharge elimination system regulation and of watershed microbial contaminants. Crit. Rev. Environ. Sci. Technol. 33:1–27. the effluent guidelines for concentrated animal feeding operations. EPA-821-R-01-003. USEPA, Washington, DC.
Environmental regulations and technology: Control Smith, Contemporary perspectives on infectious disease agents in of pathogens and vector attraction in sewage sludge sewage sludge and manure
  • Usepa J E Jr
  • P Millner
  • W Jakubowski
  • N Goldstein
  • R Rynk
USEPA. 1999. Environmental regulations and technology: Control Smith, J.E., Jr., P. Millner, W. Jakubowski, N. Goldstein, and R. Rynk. 2004. Contemporary perspectives on infectious disease agents in of pathogens and vector attraction in sewage sludge. EPA/625/ R-92/013. USEPA, Washington, DC. sewage sludge and manure. The JG Press, Emmaus, PA.
Wastewater reclamation criteria. California tific group
  • California State
State of California. 1978. Wastewater reclamation criteria. California tific group. WHO Tech. Rep. Ser. 778. WHO, Geneva.
Assessment of methods for detection of infectious Cryptosporidium oocysts and Giardia cysts in reclaimed effluents. ters 4 and 11
  • W Quintero-Betancourt
  • A L Gennaccaro
  • T M Scott
  • J B Usda
Quintero-Betancourt, W., A.L. Gennaccaro, T.M. Scott, and J.B. USDA. 1992. National engineering handbook: Agricultural waste management field handbook. Part 651 (210-AWMFH, 4/92). Chap-Rose. 2003. Assessment of methods for detection of infectious Cryptosporidium oocysts and Giardia cysts in reclaimed effluents. ters 4 and 11. USDA, Washington, DC.
Removal of pathogenic and indicator microorganisms by a full-scale
  • L J Dickson
  • S R Farrah
  • R P Carahan
USEPA. 1996b. Clean Water Needs Survey report to Congress Rose, J.B., L.J. Dickson, S.R. Farrah, and R.P. Carahan. 1996. Removal of pathogenic and indicator microorganisms by a full-scale [Online]. Available at www.epa.gov/owm/mtb/cwns/1996rtc/toc.htm (verified 11 Nov. 2004). USEPA, Washington, DC. water reclamation facility. Water Res. 30:2785-2797.
Microbiological aerosols from the application of World Health Organization. 1989. Health guidelines for the use of wastewater in agriculture and aquaculture
  • C A Sorber
  • B E Moore
  • D E Johnson
  • H J Harding
  • R F Thomas
Sorber, C.A., B.E. Moore, D.E. Johnson, H.J. Harding, and R.F. Thomas. 1984. Microbiological aerosols from the application of World Health Organization. 1989. Health guidelines for the use of wastewater in agriculture and aquaculture. Report of a WHO scienliquid sludge to land. J. Water Pollut. Control Fed. 56:830-836. State of California. 1978. Wastewater reclamation criteria. California tific group. WHO Tech. Rep. Ser. 778. WHO, Geneva.
Japan, may be food-borne, as suggested by the presence of hepatitis E virus in pig liver as food
  • Hokkaido
tis E in Hokkaido, Japan, may be food-borne, as suggested by the presence of hepatitis E virus in pig liver as food. J. Gen. Virol. 84: United States Census Bureau. 1999. National data chart for total occupied housing units [Online]. Available at www.census.gov/hhes/ 2351-2357.