• 1.

    Wilkinson KG. The biosecurity of on-farm mortality composting. J Appl Microbiol 2007;102:609618.

  • 2.

    Carcass disposal: a comprehensive review. Available at: fss.kstate.edu/FeaturedContent/CarcassDisposal/CarcassDisposal.htm. Mar 17, 2008.

    • Search Google Scholar
    • Export Citation
  • 3.

    Sander JE, Warbington MC, Myers LM. Selected methods of animal carcass disposal. J Am Vet Med Assoc 2002;220:10031005.

  • 4.

    Keener HM, Foster SS, Moeller SJ. Ohio's farmstead composting program—a decade of success. Available at: www.oardc.ohiostate.edu/ocamm/Keener-Maine%20Mortality%20Paper%205-24-05.pdf. Mar 17, 2008.

    • Search Google Scholar
    • Export Citation
  • 5.

    Jones PW. Health hazards associated with the handling of animal wastes. Vet Rec 1980;106:47.

  • 6.

    Integrated animal waste management. Task Force report No. 128. Ames, Iowa: Council for Agricultural Science and Technology, 1996.

  • 7.

    Composting for manure management. BioCycle report. Emmaus, Pa: JG Press Inc, 1998.

  • 8.

    Chapter 4: composting methods. In: Rynk R, ed. On-farm composting handbook. Ithaca, NY: Northeast Regional Agricultural Engineering Service, 1992;2440.

    • Search Google Scholar
    • Export Citation
  • 9.

    FOXNews.com. California heat wave causes livestock carcass pileup. Available at: www.foxnews.com/story/02933205661,00.html. Mar 17, 2008.

    • Search Google Scholar
    • Export Citation
  • 10.

    Title 21 Code of Federal Regulations 589.2000. Available at www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfCFR/CFRSearch.cfm?fr=589.2000. Sep 3, 2008.

    • Search Google Scholar
    • Export Citation
  • 11.

    On-farm composting: a review of the literature. Available at: www1.agric.gov.ab.ca/$department/deptdocs.nsf/all/sag2147?opendocument. Mar 17, 2008.

    • Search Google Scholar
    • Export Citation
  • 12.

    Farm-Scale composting resource list. Available at: attra.ncat.org/attra-pub/farmcompost.html. Mar 17, 2008.

  • 13.

    Compost Research Group. OARDC FABE. Available at: www.oardc.ohio-state.edu/michel/CompostResearch.htm. Mar 17, 2008.

  • 14.

    Kalbasi A, Mukhtar S, Hawkins SE, et al. Carcass composting for management of farm mortalities: a review. Compost Sci Util 2005;13:180193.

    • Search Google Scholar
    • Export Citation
  • 15.

    Kalbasi A, Mukhtar S, Hawkins SE, et al. Design, utilization, biosecurity, environmental and economic considerations of carcass composting. Compost Sci Util 2006;14:90102.

    • Search Google Scholar
    • Export Citation
  • 16.

    Spencer JL, Rennie B, Guan J. Emphasis on biosecurity for composting poultry and manure during an outbreak of highly pathogenic avian influenza in British Colombia. Can Anim Health Net Bull 2004;9:2123.

    • Search Google Scholar
    • Export Citation
  • 17.

    Prevalence of persistence of pathogens in New York State roadkill disposed of through composting: a literature review. Available at: cwmi.css.cornell.edu/. Mar 17, 2008.

    • Search Google Scholar
    • Export Citation
  • 18.

    Cekmecelioglu D, Demirci A, Graves RE. Feedstock optimization of in-vessel food waste composting systems for inactivation of pathogenic microorganisms. J Food Prot 2005;68:589596.

    • Search Google Scholar
    • Export Citation
  • 19.

    Nakasaki K, Sasaki M, Shoda M, et al. Effect of seeding during thermophilic composting of sewage sludge. Appl Environ Microbiol 1985;49:724726.

    • Search Google Scholar
    • Export Citation
  • 20.

    Nakasaki K, Sasaki M, Shoda M, et al. Characteristics of mesophilic bacteria isolated during thermophilic composting of sewage sludge. Appl Environ Microbiol 1985;49:4245.

    • Search Google Scholar
    • Export Citation
  • 21.

    Nakasaki K, Nag K, Karita S. Microbial succession associated with organic matter decomposition during thermophilic composting of organic waste. Waste Manag Res 2005;23:4856.

    • Search Google Scholar
    • Export Citation
  • 22.

    Glanville TD, Trampel DW. Composting alternative for animal carcass disposal. J Am Vet Med Assoc 1997;210:11161120.

  • 23.

    Nakasaki K, Shoda M, Kubota H. Effect of temperature on composting of sewage sludge. Appl Environ Microbiol 1985;50:15261530.

  • 24.

    Haug RT. Practical handbook of compost engineering. Ann Arbor, Mich: Lewis Publishers, 1993.

  • 25.

    Nakasaki K, Yagushi H, Sasaki Y, et al. Effects of pH control on composting of garbage. Waste Manag Res 1993;11:117125.

  • 26.

    Glanville TD, Richard TL, Harmon JD, et al. Environmental impact and biosecurity of composting for emergency disposal of livestock mortalities. Final project report for Iowa Department of Natural Resources. Ames, Iowa: Iowa State University, 2006.

    • Search Google Scholar
    • Export Citation
  • 27.

    Ahn HK, Richard TL, Glanville TD, et al. Laboratory determination of compost physical parameters for modeling airflow characteristics. Waste Manag 2008;28:660670.

    • Search Google Scholar
    • Export Citation
  • 28.

    Keener HM, Elwell DL, Monnin MJ. Procedures and equations for sizing of structures and windrows for composting animal mortalities. Appl Eng Agric 2000;16:681692.

    • Search Google Scholar
    • Export Citation
  • 29.

    Sikora LJ, Francis H. Building a pad from lime-stabilized soil. Biocycle 2000;41:4547.

  • 30.

    Sorqvist S. Heat resistance in liquids of Enterococcus spp., Listeria spp., Escherichia coli, Yersinia enterocolitica, Salmonella spp. and Campylobacter spp. Acta Vet Scand 2003;44:119.

    • Search Google Scholar
    • Export Citation
  • 31.

    Byrne B, Dunne G, Bolton DJ. Thermal inactivation of Bacillus cereus and Clostridium perfringens vegetative cells and spores in pork luncheon roll. Food Microbiol 2006;23:803808.

    • Search Google Scholar
    • Export Citation
  • 32.

    International Commission of Microbiological Specifications for Foods (ICMSF). Microbiological specifications of food pathogens. In: Microorganisms in foods 5: characteristics of microbial pathogens. London: Blackie Academic & Professional, 1996;66111.

    • Search Google Scholar
    • Export Citation
  • 33.

    Rose JB, Slifko TR. Giardia, Cryptosporidium, and Cyclospora and their impact on foods: a review. J Food Prot 1999;62:10591070.

  • 34.

    Day M, Shaw K. Biological, chemical and physical processes of composting. In: Stofella P, Kahn B, eds. Compost utilization in horticultural cropping systems. Boca Raton, Fla: Lewis Publishers, 2000;1750.

    • Search Google Scholar
    • Export Citation
  • 35.

    Burge WD, Enkiri NK, Hussong D. Salmonella regrowth in compost as influenced by substrate. Microb Ecol 1987;14:243253.

  • 36.

    Jiang X, Morgan J, Doyle MP. Thermal inactivation of Escherichia coli O157:H7 in cow manure compost. J Food Prot 2003;66:17711777.

  • 37.

    Jiang X, Morgan J, Doyle MP. Fate of Escherichia coli O157:H7 during composting of bovine manure in a laboratory-scale bioreactor. J Food Prot 2003;66:2530.

    • Search Google Scholar
    • Export Citation
  • 38.

    Lung AJ, Lin CM, Kim JM, et al. Destruction of Escherichia coli O157:H7 and Salmonella enteritidis in cow manure composting. J Food Prot 2001;64:13091314.

    • Search Google Scholar
    • Export Citation
  • 39.

    Mohee R, Driver MF, Sobratee N. Transformation of spent broiler litter from exogenous matter to compost in a sub-tropical context. Bioresour Technol 2008;99:128136.

    • Search Google Scholar
    • Export Citation
  • 40.

    Hassen A, Belguith K, Jedidi N, et al. Microbial characterization during composting of municipal solid waste. Bioresour Technol 2001;80:217225.

    • Search Google Scholar
    • Export Citation
  • 41.

    Johannessen GS, James CE, Allison HE, et al. Survival of a Shiga toxin-encoding bacteriophage in a compost model. FEMS Microbiol Lett 2005;245:369375.

    • Search Google Scholar
    • Export Citation
  • 42.

    Muniesa M, Lucena F, Jofre J. Comparative survival of free shiga toxin 2-encoding phages and Escherichia coli strains outside the gut. Appl Environ Microbiol 1999;65:56155618.

    • Search Google Scholar
    • Export Citation
  • 43.

    Russ CF, Yanko WA. Factors affecting salmonellae repopulation in composted sludges. Appl Environ Microbiol 1981;41:597602.

  • 44.

    Mote CR, Emerton BL, Allison JS, et al. Survival of coliform bacteria in static compost piles of dairy waste solids intended for freestall bedding. J Dairy Sci 1988;71:16761681.

    • Search Google Scholar
    • Export Citation
  • 45.

    Thompson WH, Leege PB, Millner PD, et al. Test methods for the examination of composting and compost (TMECC) on CD, June 2002. Holbrook, NY: The Composting Council Research and Education Foundation. Available at: tmecc.org/. Mar 17, 2008.

    • Search Google Scholar
    • Export Citation
  • 46.

    Hussong D, Burge WD, Enkiri NK. Occurrence, growth, and suppression of salmonellae in composted sewage sludge. Appl Environ Microbiol 1985;50:887893.

    • Search Google Scholar
    • Export Citation
  • 47.

    Lang N, Smith S, Bellett-Travers DM, et al. Decay of Escherichia coli in soil following the application of biosolids to agricultural land. Water Environ Manage J 2003;17:2328.

    • Search Google Scholar
    • Export Citation
  • 48.

    Millner PD, Powers KE, Enkiri NK, et al. Microbially mediated growth and suppression and death of Salmonella in composted sewage sludge. Microb Ecol 1987;14:225265.

    • Search Google Scholar
    • Export Citation
  • 49.

    Zaleski KJ, Josephson KL, Gerba CP, et al. Potential regrowth and recolonization of salmonellae and indicators in biosolids and biosolid-amended soil. Appl Environ Microbiol 2005;71:37013708.

    • Search Google Scholar
    • Export Citation
  • 50.

    Sidhu J, Gibbs RA, Ho GE, et al. Selection of Salmonella typhimurium as an indicator for pathogen regrowth potential in composted biosolids. Lett Appl Microbiol 1999;29:303307.

    • Search Google Scholar
    • Export Citation
  • 51.

    Sidhu J, Gibbs RA, Ho GE, et al. The role of indigenous microorganisms in suppression of Salmonella regrowth in composted biosolids. Water Res 2001;35:913920.

    • Search Google Scholar
    • Export Citation
  • 52.

    Déportes I, Benoit-Guyod JL, Zmirou D, et al. Microbial disinfection capacity of municipal solid waste (MSW) composting. J Appl Microbiol 1998;85:238246.

    • Search Google Scholar
    • Export Citation
  • 53.

    Zaleski KJ, Josephson KL, Gerba CP, et al. Potential regrowth and recolonization of salmonellae and indicators in biosolids and biosolid-amended soil. Appl Environ Microbiol 2005;71:37013708.

    • Search Google Scholar
    • Export Citation
  • 54.

    Droffner ML, Brinton WF. Survival of E. coli and Salmonella populations in aerobic thermophilic composts as measured with DNA gene probes. Zentralbl Hyg Umweltmed 1995;197:387397.

    • Search Google Scholar
    • Export Citation
  • 55.

    Pourcher AM, Morand P, Picard-Bonnaud F, et al. Decrease of enteric micro-organisms from rural sewage sludge during their composting in straw mixture. J Appl Microbiol 2005;99:528539.

    • Search Google Scholar
    • Export Citation
  • 56.

    Bohnel H, Lube K. Clostridium botulinum and bio-compost. A contribution to the analysis of potential health hazards caused by bio-waste recycling. J Vet Med B Infect Dis Vet Public Health 2000;47:785795.

    • Search Google Scholar
    • Export Citation
  • 57.

    Critchley EM. A comparison of human and animal botulism: a review. J R Soc Med 1991;84:295298.

  • 58.

    Staempfli H, Oliver O. Disease caused by Clostridium species. In: Howard J, ed. Current veterinary therapy 3. Philadelphia: WB Saunders Co, 1993;568569.

    • Search Google Scholar
    • Export Citation
  • 59.

    Wells C, Wilkins T. Clostridia: spore-forming anaerobic bacilli. In: Baron M, ed. Medical microbiology. 4th ed. Galveston, Tex: The University of Texas Medical Branch, 2008. Available at: www.ncbi.nlm.nih.gov/books/bv.fcgi?rid=mmed.chapter.1050. Sep 17, 2008.

    • Search Google Scholar
    • Export Citation
  • 60.

    Graham JM. Inhibition of Clostridium botulinum type C by bacteria isolated from mud. J Appl Bacteriol 1978;45:205211.

  • 61.

    Sandler RJ, Rocke TE, Samuel MD, et al. Seasonal prevalence of Clostridium botulinum type C in sediments of a northern California wetland. J Wildl Dis 1993;29:533539.

    • Search Google Scholar
    • Export Citation
  • 62.

    Smith LD. Inhibition of Clostridium botulinum by strains of Clostridium perfringens isolated from soil. Appl Microbiol 1975;30:319323.

    • Search Google Scholar
    • Export Citation
  • 63.

    Kelch WJ, Kerr LA, Pringle JK, et al. Fatal Clostridium botulinum toxicosis in eleven Holstein cattle fed round bale barley haylage. J Vet Diagn Invest 2000;12:453455.

    • Search Google Scholar
    • Export Citation
  • 64.

    Sandler RJ, Rocke TE, Yuill TM. The inhibition of Clostridium botulinum type C by other bacteria in wetland sediments. J Wildl Dis 1998;34:830833.

    • Search Google Scholar
    • Export Citation
  • 65.

    Allison MJ, Maloy SE, Matson RR. Inactivation of Clostridium botulinum toxin by ruminal microbes from cattle and sheep. Appl Environ Microbiol 1976;32:685688.

    • Search Google Scholar
    • Export Citation
  • 66.

    Grecz N, Arvay LH. Effect of temperature on spore germination and vegetative cell growth of Clostridium botulinum. Appl Environ Microbiol 1982;43:331337.

    • Search Google Scholar
    • Export Citation
  • 67.

    Gale P. Risks to farm animals from pathogens in composted catering waste containing meat. Vet Rec 2004;155:7782.

  • 68.

    Gale P. Risk assessment: use of composting and biogas treatment to dispose of catering waste containing meat. Final report to the department for environment, food and rural affairs (DEFRA). London: DEFRA, WRc-NSF Ltd, 2008.

    • Search Google Scholar
    • Export Citation
  • 69.

    Grewal SK, Rajeev S, Sreevatsan S, et al. Persistence of Mycobacterium avium subsp paratuberculosis and other zoonotic pathogens during simulated composting, manure packing, and liquid storage of dairy manure. Appl Environ Microbiol 2006;72:565574.

    • Search Google Scholar
    • Export Citation
  • 70.

    Wright PE, Inglis SF, Stehman SM, et al. Reduction of selected pathogens in anaerobic digestion. Available at: www.manuremanagement.cornell.edu/docs/. on Mar 17, 2008.

    • Search Google Scholar
    • Export Citation
  • 71.

    Monteith HD, Shannon EE, Derbyshire JB. The inactivation of a bovine enterovirus and a bovine parvovirus in cattle manure by anaerobic digestion, heat treatment, gamma irradiation, ensilage and composting. J Hyg (Lond) 1986;97:175184.

    • Search Google Scholar
    • Export Citation
  • 72.

    Huang H, Spencer JL, Soutyrine A, et al. Evidence for degradation of abnormal prion protein in tissues from sheep with scrapie during composting. Can J Vet Res 2007;71:3440.

    • Search Google Scholar
    • Export Citation
  • 73.

    Gale P, Stanfield G. Towards a quantitative risk assessment for BSE in sewage sludge. J Appl Microbiol 2001;91:563569.

  • 74.

    McQuiston JH, Garber LP, Porter-Spalding BA, et al. Evaluation of risk factors for the spread of low pathogenicity H7N2 avian influenza virus among commercial poultry farms. J Am Vet Med Assoc 2005;226:767772.

    • Search Google Scholar
    • Export Citation
  • 75.

    ProMED 2/5/2007—anthrax, human, bovine—Australia (Victoria). Available at: www.promedmail.org/pls/otn/f?p=2400:1202:3759577525819148:NO:F2400_P1202_CHECK_DISPLAY,F2400_P1202_PUB_MAIL_ID:X,36236. Sept 3, 2008.

    • Search Google Scholar
    • Export Citation
  • 76.

    ProMED 9/5/2007—anthrax, bovine—Russia (Buryatia). Available at: www.promedmail.org/pls/otn/f?p=2400:1202:1423323494241309:NO:F2400_P1202_CHECK_DISPLAY,F2400_P1202_PUB_MAIL_ID:X,39149. Sept 3, 2008.

    • Search Google Scholar
    • Export Citation
  • 77.

    Scientific Panel on Biological Hazards of the European Food Safety Authority. Opinion of the Scientific Panel on Biological Hazards of the European Food Safety Authority on the safety vis-à-vis biological risks of biogas and compost treatment standards of animal by-products (ABP). EFSA J 2005;264:121.

    • Search Google Scholar
    • Export Citation
  • 78.

    Tonner-Klank L, Moller J, Forslund A, et al. Microbiological assessments of compost toilets: in situ measurements and laboratory studies on the survival of fecal microbial indicators using sentinel chambers. Waste Manag 2006;27:11441154.

    • Search Google Scholar
    • Export Citation
  • 79.

    Vinnerås B. Comparison of composting, storage and urea treatment for sanitising of faecal matter and manure. Bioresour Technol 2007;98:33173321.

    • Search Google Scholar
    • Export Citation
  • 80.

    Vinnerås B, Björklund A, Jönsson H. Thermal composting of faecal matter as treatment and possible disinfection method–laboratory-scale and pilot-scale studies. Bioresour Technol 2003;88:4754.

    • Search Google Scholar
    • Export Citation
  • 81.

    Smårs S. An advanced experimental composting reactor for systematic simulation studies. J Agric Eng Res 2001;78:415422.

  • 82.

    Smårs S, Gustafsson L, Beck-Friis B, et al. Improvement of the composting time for household waste during an initial low pH phase by mesophilic temperature control. Bioresour Technol 2002;84:237241.

    • Search Google Scholar
    • Export Citation
  • 83.

    Christensen KK, Carlsbaek M, Kron E. Strategies for evaluating the sanitary quality of composting. J Appl Microbiol 2002;92:11431158.

  • 84.

    Pillai SD, Widmer KW, Dowd SE, et al. Occurrence of airborne bacteria and pathogen indicators during land application of sewage sludge. Appl Environ Microbiol 1996;62:296299.

    • Search Google Scholar
    • Export Citation

Advertisement

Methods and microbial risks associated with composting of animal carcasses in the United States

View More View Less
  • 1 Department of Clinical Sciences, College of Veterinary Medicine, Washington State University, Pullman, WA 99164.
  • | 2 Department of Agricultural & Biosystems Engineering, Iowa State University, Ames, IA 50011.
  • | 3 USDA-ARS-BARC-Sustainable Agricultural Systems and Food Safety Laboratories, BLDG 001, Room 122, BARC-West, Beltsville, MD 20705.
  • | 4 Veterinary Medicine Extension, School of Veterinary Medicine, University of California, Davis, CA 95616.

Contributor Notes

Supported by a grant from the Department of Homeland Security National Center for Foreign Animal and Zoonotic Disease Defense.

Address correspondence to Dr. Klingborg.