Persistence of Clostridium difficile in wastewater treatment-derived biosolids during land application or windrow composting

Journal of Applied Microbiology

Volumn 120, Issue 2, 2016, Pages 312-320

  Xu, C ^a   Wang, D ^a   Huber, A ^b   Weese, S J ^c   Warriner, Keith ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b Soil Resource Group   (Canada)

^c UNIVERSITY OF GUELPH   (Canada)

Author keywords

Biosolids; Clostridium difficile; Community associated CDI; Endospores; Loam; Persistence; Sandy loam; Windrow composting

Indexed keywords

ANAEROBIC DIGESTION; BIOLOGICAL MATERIALS; CLOSTRIDIUM; SOILS; WASTEWATER TREATMENT;

AGRICULTURAL SOILS; CLIMATIC CONDITIONS; CLOSTRIDIUM DIFFICILE; COMMUNITY-ASSOCIATED CDI; ENDOSPORE; LAND APPLICATIONS; LOAM; PERSISTENCE; SANDY LOAMS; WINDROW COMPOSTING;

BIOSOLIDS;

AGRICULTURAL SOIL; ANOXIC CONDITIONS; BACTERIUM; BIOSOLID; COMPOSTING; DIGESTIBILITY; ENVIRONMENTAL CONDITIONS; LOAM; PERSISTENCE; SANDY LOAM; SEASONAL VARIATION; SPORE; WASTEWATER; WATER TREATMENT;

BACTERIAL SPORE; BIOSOLID; COMPOSTING; CONTROLLED STUDY; HUMAN; PEPTOCLOSTRIDIUM DIFFICILE; SANDY LOAM; SPRING; SUMMER; WASTE WATER MANAGEMENT; CHEMISTRY; EVALUATION STUDY; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; PROCEDURES; RIBOTYPING; SEWAGE; SOIL; WASTE DISPOSAL; WASTE WATER;

CLOSTRIDIUM DIFFICILE;

SEWAGE; SOIL; WASTE WATER;

CLOSTRIDIUM DIFFICILE; REFUSE DISPOSAL; RIBOTYPING; SEWAGE; SOIL; SOIL MICROBIOLOGY; SPORES, BACTERIAL; WASTE WATER;

EID: 84955311777     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.13018     Document Type: Article

References (40)

1. Apedaile, E. (2001) A perspective on biosolids management. Can J Infect Dis 12, 202-204.
2. van Asselt, E.D. and Zwietering, M.H. (2006) A systematic approach to determine global thermal inactivation parameters for various food pathogens. Int J Food Microbiol 107, 73-82.
3. Berry, E.D., Millner, P.D., Wells, J.E., Kalchayanand, N. and Guerini, M.N. (2013) Fate of naturally occurring Escherichia coli O157:H7 and other zoonotic pathogens during minimally managed bovine feedlot manure composting processes. J Food Prot 76, 1308-1321.
4. Bradford, S.A., Morales, V.L., Zhang, W., Harvey, R.W., Packman, A.I., Mohanram, A. and Welty, C. (2013) Transport and fate of microbial pathogens in agricultural settings. Crit Rev Environ Sci Technol 43, 775-893.
5. Brochier, V., Gourland, P., Kallassy, M., Poitrenaud, M. and Houot, S. (2012) Occurrence of pathogens in soils and plants in a long-term field study regularly amended with different composts and manure. Agric Ecosyst Environ 160, 91-98.
6. Brodie, H.L., Carr, L.E. and Condon, P. (2000) A comparison of static pile and turned windrow methods for poultry litter compost production. Compost Sci Util 8, 178-189.
7. Costa, M.C., Reid-Smith, R., Gow, S., Hannon, S.J., Booker, C., Rousseau, J., Benedict, K.M., Morley, P.S. et al. (2012) Prevalence and molecular characterization of Clostridium difficile isolated from feedlot beef cattle upon arrival and mid-feeding period. BMC Vet Res 8, 1-4.
8. Delate, T., Albrecht, G., Won, K. and Jackson, A. (2015) Ambulatory-treated Clostridium difficile infection: a comparison of community-acquired vs. nosocomial infection. Epidemiol Infect 143, 1225-1235.
9. Deng, K., Plaza-Garrido, A., Torres, J.A. and Paredes-Sabja, D. (2015) Survival of Clostridium difficile spores at low temperatures. Food Microbiol 46, 218-221.
10. Desmarais, T.R., Solo-Gabriele, H.M. and Palmer, C.J. (2002) Influence of soil on fecal indicator organisms in a tidally influenced subtropical environment. Appl Environ Microbiol 68, 1165-1172.
11. Evans, C.T. and Safdar, N. (2015) Current trends in the epidemiology and outcomes of Clostridium difficile infection. Clin Infect Dis 60, S66-S71.
12. Gozen, I. and Ormeci, B. (2010) Effect of daylight on regrowth of bacteria in anaerobically digested sludge. Water Sci Technol 62, 364-369.
13. Hassen, A., Belguith, K., Jedidi, N., Cherif, A., Cherif, M. and Boudabous, A. (2001) Microbial characterization during composting of municipal solid waste. Bioresour Technol 80, 217-225.
14. Islam, M., Morgan, J., Doyle, M.P., Phatak, S.C., Millner, P. and Jiang, X. (2004) Persistence of Salmonella enterica serovar Typhimurium on lettuce and parsley and in soils on which they were grown in fields treated with contaminated manure composts or irrigation water. Foodborne Pathog Dis 1, 27-35.
15. Karpowicz, E., Novinscak, A., Barlocher, F. and Filion, M. (2010) qPCR quantification and genetic characterization of Clostridium perfringens populations in biosolids composted for 2 years. J Appl Microbiol 108, 571-581.
16. Khanna, S., Pardi, D.S., Aronson, S.L., Kammer, P.P., Orenstein, R., St Sauver, J.L., Harmsen, W.S. and Zinsmeister, A.R. (2012) The Epidemiology of community-acquired Clostridium difficile Infection: a population-based study. Am J Gastroenterol 107, 89-95.
17. Klein, M., Brown, L., Ashbolt, N.J., Stuetz, R.M. and Roser, D.J. (2011) Inactivation of indicators and pathogens in cattle feedlot manures and compost as determined by molecular and culture assays. FEMS Microbiol Ecol 77, 200-210.
18. Lang, N.L., Smith, S.R., Bellett-Travers, D.M., Pike, E.B. and Rowlands, C.L. (2003) Decay of Escherichia coli in soil following the application of biosolids to agricultural land. Water Environ J 17, 23-28.
19. Lu, Q., He, Z.L. and Stoffella, P.J. (2012) Land application of biosolids in the USA: a review. Appl Environ Soil Sci 2012, 1-11.
20. Magri, A. and Teira-Esmatges, M.R. (2015) Assessment of a composting process for the treatment of beef cattle manure. J Environ Sci Health B 50, 430-438.
21. Mantovi, P., Baldoni, G. and Toderi, G. (2005) Reuse of liquid, dewatered, and composted sewage sludge on agricultural land: effects of long-term application on soil and crop. Water Res 39, 289-296.
22. Marsh, J.W., Tulenko, M.M., Shutt, K.A., Thompson, A.D., Weese, J.S., Songer, J.G., Limbago, B.M. and Harrison, L.H. (2011) Multi-locus variable number tandem repeat analysis for investigation of the genetic association of Clostridium difficile isolates from food, food animals and humans. Anaerobe 17, 156-160.
23. Mc Carthy, G., Lawlor, P.G., Coffey, L., Nolan, T., Gutierrez, M. and Gardiner, G.E. (2011) An assessment of pathogen removal during composting of the separated solid fraction of pig manure. Bioresour Technol 102, 9059-9067.
24. Metcalf, D.S., Costa, M.C., Dew, W.M.V. and Weese, J.S. (2010) Clostridium difficile in vegetables, Canada. Lett Appl Microbiol 51, 600-602.
25. Ontario Ministry of the Environment (2012) Ontario Compost Quality Standards. Available at http://www.ewswa.org/wp-content/uploads/2011/06/Ontario-Compost-Standards.pdf (accessed July 2015).
26. Pourcher, A.M., Morand, P., Picard-Bonnaud, F., Billaudel, S., Monpoeho, S., Federighi, M., Ferre, V. and Moguedet, G. (2005) Decrease of enteric micro-organisms from rural sewage sludge during their composting in straw mixture. J Appl Microbiol 99, 528-539.
27. Pourcher, A.M., Françoise, P.B., Virginie, F., Agnieszka, G., Vasilica, S. and Gérard, M. (2007) Survival of faecal indicators and enteroviruses in soil after land-spreading of municipal sewage sludge. Appl Soil Ecol 35, 473-479.
28. Robertson, L.J. and Gjerde, B.K. (2004) Effects of the Norwegian winter environment on Giardia cysts and Cryptosporidium oocysts. Microb Ecol 47, 359-365.
29. Rodriguez-Palacios, A., Reid-Smith, R.J., Staempfli, H.R. and Weese, J.S. (2010) Clostridium difficile survives minimal temperature recommended for cooking ground meats. Anaerobe 16, 540-542.
30. Rouch, D.A., Mondal, T., Pai, S., Glauche, F., Fleming, V.A., Thurbon, N., Blackbeard, J., Smith, S.R. et al. (2011) Microbial safety of air-dried and rewetted biosolids. J Water Health 9, 403-414.
31. Rupnik, M. and Songer, J.G. (2010) Clostridium difficile: its potential as a source of foodborne disease. Adv Food Nutr Res 60, 53-66.
32. Ryckeboer, J., Mergaert, J., Vaes, K., Klammer, S., De Clercq, D., Coosemans, J., Insam, H. and Swings, J. (2003) A survey of bacteria and fungi occurring during composting and self-heating processes. Ann Microbiol 53, 349-410.
33. Salsali, H., Parker, W.J. and Sattar, S.A. (2008) The effect of volatile fatty acids on the inactivation of Clostridium perfringens in anaerobic digestion. World J Microbiol Biotechnol 24, 659-665.
34. Stefanis, C., Alexopoulos, A., Voidarou, C., Vavias, S. and Bezirtzoglou, E. (2014) Prevalence of C. perfringens in agricultural fields with different vegetation types. Folia Microbiol 59, 1-4.
35. Tsadilas, C.D., Mitsios, I.K. and Golia, E. (2005) Influence of biosolids application on some soil physical properties. Commun Soil Sci Plant Anal 36, 709-716.
36. Wang, S.W., Shen, A.M., Setlow, P. and Li, Y.Q. (2015) Characterization of the dynamic germination of individual Clostridium difficile spores using Raman spectroscopy and differential interference contrast microscopy. J Bacteriol 197, 2361-2373.
37. Weese, J.S. (2011) Bacterial enteritis in dogs and cats: diagnosis, therapy, and zoonotic potential. Vet Clin North Am Small Anim Pract 41, 287-292.
38. Xu, C., Weese, J.S., Flemming, C., Odumeru, J. and Warriner, K. (2014) Fate of Clostridium difficile during wastewater treatment and incidence in Southern Ontario watersheds. J Appl Microbiol 117, 891-904.
39. Yucel, D., Yucel, C., Aksakal, E.L., Barik, K., Khosa, M., Aziz, I. and Islam, K.R. (2015) Impacts of biosolids application on soil quality under alternate year no-till corn-soybean rotation. Water Air Soil Pollut 226, 1-11.
40. Zaleski, K.J., Josephson, K.L., Gerba, C.P. and Pepper, I.L. (2005) Survival, growth, and regrowth of enteric indicator and pathogenic bacteria in biosolids, compost, soil, and land applied biosolids. J Residuals Sci Technol 2, 49-63.