Skip to main content
SpringerLink
Log in

Reduction of Pathogens in Bovine Manure in Three Full-scale Commercial Anaerobic Digesters

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

Two field studies were conducted to determine the effect of anaerobic digestion (AD) on the presence and levels of pathogens in post-AD materials. In the first study, samples of pre-AD liquid, post-AD liquid, and post-AD solid were assayed bi-weekly, for six sampling events from a continuous mix and plug-flow AD. In the second study, samples were taken from multiple locations pre-AD and post-AD before and after liquid-solid separation. Samples were assayed for generic E. coli (GEC), Enterococci, Mycobacterium avium subsp. paratuberculosis (MAP), bovine Enterovirus, Campylobacter spp., and Salmonella spp., Escherichia coli O157:H7. Anaerobic digestion resulted in declines of 99% for GEC and 85 to 95% for Enterococci. Twenty-five samples of composted solid manure from the plug-flow digesters indicated a reduction of > 99% for GEC and > 99% for Enterococci. Bovine Enterovirus and MAP were isolated on numerous occasions from both pre- and post-digestion samples and composted material. Salmonella spp. and Campylobacter were found in 50 to 92% both post-digestion, and remained at a detection level of 21 to 96%, respectively, in liquid manure immediately post-AD. Composting of AD solids did reduce the detection of Salmonella to 10% and Campylobacter to 0%. While substantial quantitative reductions occurred for GEC and Enterococci, the minimal survival of these indicator organisms along with the frequent survival of Enterovirus and MAP indicates that AD, even followed by composting, would not remove all biosecurity hazards.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Adhikara, B., Besser, T. E., Gay, J. M., Fox, L. K., Davis, M. A., Cobbold, R. N., Berge, A. C., & Hancock, D. D. (2009). The role of animal movement, including off-farm rearing of heifers, in the interherd transmission of multidrug-resistant Salmonella. Journal of Dairy Science, 92, 4229–4238. https://doi.org/10.3168/jds.2008-1494.

    Article  CAS  Google Scholar 

  • A.P.H.A. 1995. Standard methods for examination of water and wastewater. 19th ed, 1995, pp 9–89 to 9–91.

  • Bagge, E., Sahlstrom, L., & Albihn, A. (2005). The effect of hygienic treatment on the microbial flora of biowaste at biogas plants. Water Research, 39, 4879–4886.

    Article  CAS  Google Scholar 

  • Bae, W., Kaya, K. N., Hancock, D. D., Call, D. R., Park, Y. H., & Besser, T. E. (2005). Prevalence and antimicrobial resistance of thermophiollic Campylobacter spp. from cattle farms in Washington state. Applied and Environmental Microbiology, 71, 169–174. https://doi.org/10.1128/AEM.71.1.169-174.2005.

    Article  CAS  Google Scholar 

  • Beuchat, L. R., & Ryu, J. H. (1997). Produce handling and processing practices. Emerging Infectious Diseases, 3(4), 459–465.

    Article  CAS  Google Scholar 

  • Davis, M. A., Hancock, D. D., Besser, T. E., Rice, D. H., Hovde, C. J., Digiacomo, R., Samadpour, M., & Call, D. R. (2003). Correlation between geographic distance and genetic similarity in an international collection of bovine faecal Escherichia coli O157:H7 isolates. Epidemiology and Infection, 131(2), 923–930.

    Article  CAS  Google Scholar 

  • Evermann, J. F., McKeirnan, A. J., Smith, A. W., Skilling, D. E., & Ott, R. L. (1985). The isolation and identification of caliciviruses from dogs with enteric infections. American Journal of Veterinary Research, 46, 218–220.

    CAS  Google Scholar 

  • Frear, C., Liao, W., Ewing, T., & Chen, S. (2011). Evaluation of co-digestion at a commercial dairy anaerobic digester. Clean—Soil, Air, Water., 39, 697–704. https://doi.org/10.1002/clen.201000316.

    Article  CAS  Google Scholar 

  • Fröschle, B., Heiermann, M., Lebuhn, M., Messelhäusser, U., & Plöchl, M. (2015). Hygiene and sanitation in biogas plants. Advances in Biochemical Engineering/Biotechnology, 151, 63–99. https://doi.org/10.1007/978-3-319-21993-6_3.

    Article  CAS  Google Scholar 

  • Gamroth, M. and Krahn, J. (2003). Development and monitoring of anaerobic digestion of dairy manure for power generation and better manure management. Report to Portland General Electric.

  • Guan, T. Y., & Holley, R. A. (2003). Pathogen survival in swine manure environments and transmission of human enteric illness: a review. Journal of Environmental Quality, 32, 383–392.

    Article  CAS  Google Scholar 

  • Inglis, G. D., McAllister, T. A., Larney, F. J., & Topp, E. (2010). Prolonged survival of Campylobacter species in bovine manure compost. Applied and Environmental Microbiology, 76(4), 1110–1119. https://doi.org/10.1128/AEM.01902-09.

    Article  CAS  Google Scholar 

  • Jiang, Y., Dennehy, C., Lawlor, P. G., Hu, Z., Yang, Q., McCarthy, G., Tan, S. P., Zhan, X., & Gardiner, G. E. (2018). Inactivation of Salmonella during co-digestion of food waste and pig manure. Waste Management., 82, 231–240.

    Article  CAS  Google Scholar 

  • Kearney, T. E., Larkinm, M. J., Frost, J. P., & Levett, P. N. (1993a). Survival of pathogenic bacteria during mesophilic anaerobic digestion of animal waste. Journal of Applied Bacteriology, 75, 215–219.

    Article  CAS  Google Scholar 

  • Kearney, T. E., Larkin, M. J., & Levett, P. N. (1993b). The effect of slurry storage and anaerobic-digestion on survival of pathogenic bacteria. Journal of Applied Bacteriology, 74, 86–93.

    Article  CAS  Google Scholar 

  • Ley, V., Higgins, J., & Fayer, R. (2002). Bovine enteroviruses as indicator of fecal contamination. Applied and Environmental Microbiology, 68, 3455–3461.

    Article  CAS  Google Scholar 

  • Lindmark, J., Eriksson, P., & Thorin, E. (2014). The effects of different mixing intensities during anaerobic digestion of the organic fraction of municipal solid waste. Waste Management, 34, 1391–1397.

    Article  Google Scholar 

  • Manyi-Loh, C. E., Manphweli, S. N., Meyer, E. L., Okoh, A. I., Makaka, G., & Simon, M. (2014). Inactivation of selected bacterial pathogens in dairy cattle manure by mesophilic anaerobic digestion (balloon type digester). International Journal of Environmental Research and Public Health, 11, 7184–7194. https://doi.org/10.3390/ijerph110707184.

    Article  Google Scholar 

  • Masse, D., Gilbert, Y., & Topp, E. (2011). Pathogen removal in farm-scale psychrophilic anaerobic digesters processing swine amnure. Bioresource Technology, 102, 641–646.

  • Monteith, H. D., Shannon, E. E., & Derbyshire, J. B. (1986). The inactivation of a bovine enterovirous and a bovine parvovirus in cattle manure by anaerobic digestion, heat treatment, gamma irradiation, ensilage, and composting. Journal of Hygiene., 97, 175–184.

    Article  CAS  Google Scholar 

  • Natvig, E. E., Ingham, S. C., Ingham, B. H., Cooperband, L. R., & Roper, T. R. (2002). Salmonella enterica serovar Typhimurium and Escherichia coli contamination of root and leaf vegetables grown in soils with incorporated bovine manure. Applied and Environmental Microbiology, 68(6), 2737–2744.

    Article  CAS  Google Scholar 

  • Pell, A. (1997). Manure and microbes: public and animal health problem? Journal of Dairy Science, 80, 2673–2681.

    Article  CAS  Google Scholar 

  • Persson, S.P.E., Bartlett, H.D., Branding, A.E., and Regan, R.W..(2016). Agricultural anaerobic digesters: design and operation. (https://extension.psu.edu/agricultural-anaerobic-digesters-design-and-operation). Accessed Dec 2018.

  • Radke, B. R., McFall, M., & Radostits, S. M. (2002). Salmonella Muenster infection in a dairy herd. The Canadian Veterinary Journal, 43(6), 443–453.

    Google Scholar 

  • Sahlstrom, L. (2003). A review of survival of pathogenic bacteria in organic waste used in biogas plants. Bioresource Technology, 87, 161–166.

    Article  CAS  Google Scholar 

  • SAS Institute. (2018). SAS system software: release 9.2 (TS2M0). Cary, NC: SAS. Institute Inc.

    Google Scholar 

  • Scott, H., Fosgate, G. T., Libal, M. C., Sneed, L. W., Erol, E., Angulo, A. B., & Jordan, E. R. (2007). Field testing fo an enhanced direct-fecal polymerase chain reaction procedure, bacterial culture of feces, and a serum enzyme-linked immunosorbent assay for detecting Mycobacterium avium subsp paratuberculosis infection in adult cattle. American Journal of Veterinary Research, 68, 236–245.

    Article  CAS  Google Scholar 

  • Sobsey, M.D., Khati, L. A., Hill, V. R., Alocilja, E., and Pillai, S. (2006). Pathogens in animal wastes and the impacts of waste management practices on their survival, transport and fate. White Papers on Animal Agriculture and the Environment. National Center for Manure & Animal Waste Management.

  • Solomon, E. B., Yaron, S., & Matthews, K. R. (2002). Transmission of Escherichia coli O157:H7 from contaminated manure and irrigation water to lettuce plant tissue and its subsequent internalization. Applied and Environmental Microbiology, 68(1), 397–400.

    Article  CAS  Google Scholar 

  • Stabel, J. R. (1997). An improved method for cultivation of Mycobacterium paratuberculosis from bovine fecal samples and comparison to three other methods. Journal of Veterinary Diagnostic Investigation, 9, 375–380.

    Article  CAS  Google Scholar 

  • USDA (2008). Info sheet: Johne’s disease on U.S. dairies, 1991–2007. Veterinary Services, Centers for Epidemiology and Animal Health. https://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy07/Dairy07_is_Johnes.pdf. Accessed Dec 2018.

  • US EPA AgStar. https://www.epa.gov/agstar/agstar-library-tools-and-resources. Accessed Dec 2018.

  • USDA APHIS. National Veterinary Testing Services Laboratories. Ames, IA.

  • Veling, J., Wilpshaar, H., Frankena, K., Bartels, C., & Barkema, H. W. (2002). Risk factors for clinical Salmonella enterica subsp. enterica serovar Typhimurium infection on Dutch dairy farms. Preventive Veterinary Medicine, 54(2), 157–168.

    Article  CAS  Google Scholar 

  • Wagner, A. O., Gstraunthaler, G., & Illmer, P. (2008). Survival of bacterial pathogens during the thermophilic anaerobic digestion of biowaste: laboratory experiments and in situ validation. Anaerobe, 14(3), 181–183.

    Article  CAS  Google Scholar 

  • Warnick, L. D., Crofton, L. M., Pelzer, K. D., & Hawkins, M. J. (2001). Risk factors for clinical salmonellosis in Virginia, USA cattle herds. Preventive Veterinary Medicine, 49(3–4), 259–275.

    Article  CAS  Google Scholar 

  • Wells, S. J. (2000). Biosecurity on dairy operations: hazards and risks. Journal of Dairy Science, 83, 2380–2386.

    Article  CAS  Google Scholar 

  • Wells, S., & Wagner, S. (2000). Herd-level risk factors for infection with Mycobaterium paratuberculosis in US dairies and association between familiararity of the herd manager with the disease or prior diagnosis of the disease in that herd and use of preventative measures. Journal of the American Veterinary Medical Association, 216, 1450–1457.

    Article  CAS  Google Scholar 

  • Xu, W., Reuter, T., Inglis, G. D., Larney, F. J., Alexander, T. W., Guan, J., et al. (2009). A biosecure composting system for disposal of cattle carcasses and manure following infectious disease outbreak. Journal of Environmental Quality, 38(2), 437–450. https://doi.org/10.2134/jeq2008.0168.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Qualco, to whom we are indebted for the use of the land and production system used in study 2.

Funding

Financial support was provided through a NRCS conservation innovation grant 68-3A75-6-134.

Author information

Authors and Affiliations

  1. Department of Animal Sciences, Washington State University, Puyallup, WA, 98371, USA

    Hannah Chiapetta, Joe Harrison & Elizabeth Whitefield

  2. Department of Veterinary Clinical Medicine, Washington State University, Pullman, WA, 99164, USA

    John Gay

  3. Integrated Research and Innovation Center, Office of Research Assurances, University of Idaho, Moscow, ID, 83844, USA

    Russ McClanahan

  4. Department of Veterinary Clinical Sciences, Washington State University, Pullman, WA, 99164, USA

    Jim Evermann

  5. Famo Feeds, Freeport, MN, 56331, USA

    Tamilee Nennich

  6. Department of Animal Sciences, Oregon State University, Corvallis, OR, 97331, USA

    Mike Gamroth

Authors
  1. Hannah Chiapetta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joe Harrison
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John Gay
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Russ McClanahan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Elizabeth Whitefield
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jim Evermann
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tamilee Nennich
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mike Gamroth
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joe Harrison.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chiapetta, H., Harrison, J., Gay, J. et al. Reduction of Pathogens in Bovine Manure in Three Full-scale Commercial Anaerobic Digesters. Water Air Soil Pollut 230, 111 (2019). https://doi.org/10.1007/s11270-019-4163-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-019-4163-4

Keywords

Search

Navigation