Inactivation of human pathogens during phase II composting of manure-based mushroom growth substrate

Journal of Food Protection

Volumn 76, Issue 8, 2013, Pages 1393-1400

  Weil, Jennifer D ^a,b   Cutter, Catherine N ^a   Beelman, Robert B ^a   Laborde, Luke F ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b Del Monte Foods   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84882251688     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X.JFP-12-508     Document Type: Article

References (60)

1. Beyer, D. M. 2003. Basic procedures for Agaricus mushroom growing. College of Agricultural Sciences. The Pennsylvania State University, University Park.
2. Beyer, D., and J. A. Pecchia. 2010. Microbes of phase II. Mushroom News 58:14-15.
3. Beyer, D. M., R. Rynk, J. Pecchia, and P. Wuest. 2000. Improving odor management on mushroom farms. Biocycle 41:60-63.
4. Bunning, V. K., R. G. Crawford, J. T. Tierney, and J. T. Peeler. 1990. Thermotolerance of Listeria monocytogenes and Salmonella typhimurium after sublethal heat shock. Appl. Environ. Microbiol. 56:3216-3219.
5. California Leafy Green Handler Marketing Board. 2012. Leafy Greens Marketing Agreement. Commodity specific food safety guidelines for the production and harvest of leafy greens. California Leafy Green Products Handler Marketing Agreement. Available at: http://www.caleafygreens.ca.gov. Accessed 4 February 2013.
6. Canadian Food Inspection Agency. 2008. Health hazard: various sliced mushroom products may contain Listeria monocytogenes. Canadian Food Inspection Agency. Available at: http://epe.lac-bac.gc.ca/100/206/301/cfia-acia/2011-09-21/ www.inspection.gc.ca/english/corpaffr/recarapp/2008/20080801ce.shtml. Accessed 4 February 2013.
7. Canadian Food Inspection Agency. 2011. Health hazard alert: certain sliced mushrooms may contain Listeria monocytogenes. Available at: http://www.inspection. gc.ca/english/corpaffr/recarapp/2011/20111210e.shtml. Accessed 4 February 2013.
8. Canadian Food Inspection Agency. 2012. Health hazard alert: certain sliced mushrooms may contain Listeria monocytogenes. Available at: http://www.inspection. gc.ca/english/corpaffr/recarapp/2012/20120813e.shtml. Accessed 4 February 2013.
9. Canadian Food Inspection Agency. 2012. Health hazard alert: certain Champs's mushrooms brand sliced Crimini mushrooms may contain Listeria monocytogenes. Available at: http://www.inspection. gc.ca/english/corpaffr/ recarapp/2012/20120927ce.shtml. Accessed 4 February 2013.
10. Cebrian, G., N. Sagarzazu, R. Pagan, S. Condon, and P. Manas. 2008. Resistance of Escherichia coli grown at different temperatures to various environmental stresses. J. Appl. Microbiol. 105:271-278.
11. Defense Logistics Agency. 2003. Georgia Ag. Department finds contaminated mushrooms. DSCP vendor recall 022-2003. U. S. Department of Defense. Available at: http://www.troopsupport.dla. mil/subs/fso/alfood/2003/vend2203.pdf. Accessed 4 February 2013.
12. Doran, G., F. Sheridan, N. Delappe, C. O'Hare, W. Anderson, G. Corbett-Feeney, and M. Cormican. 2005. Salmonella enterica serovar Kedougou contamination of commercially grown mushrooms. Diagn. Microbiol. Infect. Dis. 51:73-76.
13. Doyle, M. E., A. S. Mazzotta, T. Wang, D. W. Wiseman, and V. N. Scott. 2001. Heat resistance of Listeria monocytogenes. J. Food Prot. 64:410-429.
14. Doyle, M. P. and J. L. Schoeni. 1986. Isolation of Campylobacter jejuni from retail mushrooms. Appl. Environ. Microbiol. 51:449-450.
15. Erickson, M., F. Critzer, and M. Doyle. 2010. Composting criteria for animal manure. Produce Safety Project Issue Brief. Pew Charitable Trusts. Available at: http://www.pewhealth.org/uploadedFiles/PHG/Content-Level-Pages/ Issue-Briefs/PSP-PEW-PSP-Composting-Manure-Narrative-v4-2.pdf. Accessed 4 February 2013.
16. Farber, J. M., and B. E. Brown. 1990. Effect of prior heat shock on heat resistance of Listeria monocytogenes in meat. Appl. Environ. Microbiol. 56:1584-1587.
17. Food Safety Authority of Ireland. 2003. Advisory Committee on the Microbiological Safety of Food-Raw mushrooms: consumer advice. Available at: http://www.food.gov. uk/multimedia/pdfs/acm655.pdf. Accessed 6 May 2013.
18. Heisick, J. E., D. E. Wagner, M. L. Nierman, and J. T. Peeler. 1989. Listeria spp. found on fresh market produce. Appl. Environ. Microbiol. 55:19251927.
19. Heuvelink, A. E., J. T. Zwartkruis-Nahuis, F. L. Van Den Biggelaar, and E. Deboer. 1996. Isolation and characterization of verocytotoxinproducing Escherichia coli O157 from slaughter pigs and poultry. Int. J. Food Microbiol. 52:67-75.
20. Himathongkham, S., and H. Riemann. 1999. Destruction of Salmonella typhimurium, Escherichia coli O157:H7 and Listeria monocytogenes in chicken manure by drying and/or gassing with ammonia. FEMS Microbiol. Lett. 171:179-182.
21. Himathongkham, S., H. Riemann, S. Bahari, S. Nuanualsuwan, P. Kass, and D. O. Cliver. 2000. Survival of Salmonella typhimurium and Escherichia coli O157:H7 in poultry manure and manure slurry at sublethal temperatures. Avian Dis. 44:853-860.
22. Ivors, K., D. Beyer, P. Wuest, and S. Kang. 2002. Survey of fungal diversity in mushroom compost using sequences of PCR-amplified genes encoding 18S ribosomal RNA, p. 17-24. In H. Insam, N. Riddech, and S. Klammer (ed.), Microbiology of composting. Springer, New York.
23. Ivors, K. L., P. D. Collopy, D. M. Beyer, and S. Kang. 2000. Identification of bacteria in mushroom compost using ribosomal RNA sequence. Compost Sci. Util. 8:247-253.
24. Jiang, X., J. Morgan, and M. P. Doyle. 2003. Thermal inactivation of Escherichia coli O157:H7 in cow manure compost. J. Food Prot. 66:1771-1777.
25. Junttila, J., and M. Brander. 1989. Listeria monocytogenes septicemia associated with consumption of salted mushrooms. Scand. J. Infect. Dis. 21:339-342.
26. Lengacher, B., T. R. Kline, L. Harpster, M. L. Williams, and J. T. Lejeune. 2010. Low prevalence of Escherichia coli O157:H7 in horses in Ohio, USA. J. Food Prot. 73:2089-2092.
27. Linton, R. H., J. B. Webster, J. D. Pierson, J. R. Bishop, and C. R. Hackney. 1992. The effect of sublethal heat shock and growth atmosphere on the heat resistance of Listeria monocytogenes Scott A. J. Food Prot. 55:84-87.
28. Murphy, R. Y., E. M. Martin, L. K. Duncan, B. L. Beard, and J. A. Marcy. 2004. Thermal process validation for Escherichia coli O157:H7, Salmonella, and Listeria monocytogenes in ground turkey and beef products. J. Food Prot. 67:1394-1402.
29. Mushroom Good Agricultural Practices. 2010. Mushroom Good Agricultural Practices-industry-wide food safety standards for fresh mushroom growing, harvesting, and shipping. American Mushroom Institute and Penn State University. Available at: http://www.mgap.org. Accessed 4 February 2013.
30. National Agricultural Statistics Service 2011. National Agricultural Statistics Service Vegetables and Melons Outlook: mushrooms. VGS-344. USDA Economic Research Service, Washington, D. C.
31. Ntougias, S., G. I. Zervakis, N. Kavroulakis, C. Ehaliotis, and K. K. Papadopoulou. 2004. Bacterial diversity in spent mushroom compost assessed by amplified rDNA restriction analysis and sequencing of cultivated isolates. Syst. Appl. Microbiol. 27:746-754.
32. Orta-Ramirez, A., and D. M. Smith. 2002. Thermal inactivation of pathogens and verification of adequate cooking in meat and poultry products. Adv. Food Nutr. Res. 44:147-194.
33. Osaili, T., C. L. Griffis, E. M. Martin, B. L. Beard, A. Keener, and J. A. Jarcy. 2006. Thermal inactivation studies of Escherichia coli O157:H7, Salmonella, and Listeria monocytogenes in ready-to-eat chicken-fried beef patties. J. Food Prot. 69:1080-1086.
34. Palma, M. A., L. A. Ribera, M. Paggi, and R. Knutson. 2010. Food safety standards for the U. S.fresh produce industry. Policy Issues P18:1-6.
35. Riemann, H., S. Himathongkham, D. Willoughby, R. Tarbell, and R. Breitmeyer. 1998. A survey for Salmonella by drag swabbing manure piles in California egg ranches. Avian Dis. 42:67-71.
36. Rossouw, W., E. Du Plessis, and L. Korsten. 2012. Microbiological quality and safety of whole white button mushrooms (Agaricus bisporus), p. 4-9. The Spawn Run. South African Mushroom Farmers' Association, Cape Town.
37. Royse, D. J., and R. B. Beelman. 2006. Six steps to mushroom farming, 2nd ed. Pennsylvania State University College of Agricultural Sciences. Available at: http://extension.psu.edu/mushroomgrowerinfo/publications/guides/SixSteps. pdf/view. Accessed 4 February 2013.
38. Samadpour, M., M. W. Barbour, T. Nguyen, T. M. Cao, F. Buck, G. A. Depavia, E. Mazengia, P. Yang, D. Alfi, M. Lopes, and J. D. Stopforth. 2006. Incidence of enterohemorrhagic Escherichia coli, Escherichia coli O157, Salmonella, and Listeria monocytogenes in retail fresh ground beef, sprouts, and mushrooms. J. Food Prot. 69:441-443.
39. Schisler, L. C. 1982. Biochemical and mycological aspects of mushroom composting, p. 3-10. In P. J. Wuest (ed.), Penn State handbook for mushroom growers. Penn State University, University Park.
40. Sergelidis, D., and A. Abrahim. 2009. Adaptive response of Listeria monocytogenes to heat and its impact on food safety. Food Control 20:1-10.
41. Singh, R., X. Jiang, and F. Luo. 2010. Thermal inactivation of heat-shocked Escherichia coli O157:H7, Salmonella, and Listeria monocytogenes in dairy compost. J. Food Prot. 73:1633-1640.
42. Singh, R., J. Kim, and X. Jiang. 2012. Heat inactivation of Salmonella spp. in fresh poultry compost by simulating early phase of composting process. J. Appl. Microbiol. 112:927-935.
43. Singh, R., J. Kim, M. W. Shepherd, Jr., F. Luo, and X. Jiang. 2011. Determining thermal inactivation of Escherichia coli O157:H7 in fresh compost by simulating early phases of the composting process. Appl. Environ. Microbiol. 77:4126-4135.
44. Sivapalasingam, S., C. R. Friedman, L. Cohen, and R. V. Tauxe. 2004. Fresh produce: a growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J. Food Prot. 67:2342-2353.
45. Strapp, C. M., A. E. H. Shearer, and R. D. Joerger. 2003. Survey of retail alfalfa sprouts and mushrooms for the presence of Escherichia coli O157:H7, Salmonella, and Listeria with BAX, and evaluation of this polymerase chain reaction-based system with experimentally contaminated samples. J. Food Prot. 66:182-187.
46. U. S. Department of Agriculture, Food Safety and Inspection Service. 2007. Isolation and identification of Listeria monocytogenes from red meat, poultry, egg, and environmental samples. U. S. Department of Agriculture, Food Safety and Inspection Service, Office of Public Health Science, Washington, D. C.
47. U. S. Food and Drug Administration. 1998. Guide to minimize microbial food safety hazards for fresh fruits and vegetables. Center for Food Safety and Applied Nutrition. Available at: http://www.fda.gov/Food/GuidanceRegulation/ GuidanceDocumentsRegulatoryInformation/ProducePlantProducts/ucm064574.htm. Accessed 6 May 2013.
48. U. S. Food and Drug Administration. 2006. Monterey Mushrooms recalls fresh sliced white and baby Bella mushrooms in PA, MD, NC, NJ, NY, OH, and VA because of possible health risk. Washington, D. C. Available at: http://www.fda.gov/Safety/Recalls/ArchiveRecalls/2006/ucm112040.htm. Accessed 4 February 2013.
49. U. S. Food and Drug Administration. 2007. Salmonella, chap. 5. In Bacteriological analytical manual, 7th ed. U. S. Food and Drug Administration, Arlington, VA.
50. U. S. Food and Drug Administration. 2008. Guidance for industry: guide to minimize microbial food safety hazards of fresh-cut fruits and vegetables. Available at: http://www.fda.gov/Food/Guidance Regulation/ GuidanceDocumentsRegulatoryInformation/ProducePlant Products/ucm064458.htm. Accessed 6 May 2013.
51. U. S. Food and Drug Administration. 2009. Guidance for industry: guide to minimize microbial food safety hazards of tomatoes; draft guidance. Available at: http://www.fda.gov/Food/GuidanceRegulation/ GuidanceDocumentsRegulatoryInformation/ProducePlantProducts/ucm173902.htm. Accessed 6 May 2013.
52. U. S. Food and Drug Administration. 2009. Guidance for industry: guide to minimize microbial food safety hazards of leafy greens; draft guidance. Available at: http://www.fda.gov/Food/GuidanceRegulation/ GuidanceDocumentsRegulatoryInformation/ProducePlantProducts/ucm174200.htm. Accessed 6 May 2013.
53. U. S. Food and Drug Administration. 2009. Guidance for industry: guide to minimize microbial food safety hazards of melons; draft guidance. Available at: http://www.fda.gov/Food/GuidanceRegulation/ GuidanceDocumentsRegulatoryInformation/ProducePlantProducts/ucm174171.htm. Accessed 6 May 2013.
54. U. S. Food and Drug Administration. 2011. Diarrheagenic Escherichia coli, chap 4A. In Bacteriological analytical manual, 8th ed. U. S. Food and Drug Administration, Arlington, VA.
55. Van Netten, P., I. Perales, A. Van De Moosdijk, G. D. W. Curtis, and D. A. A. Mossel. 1989. Liquid and solid selective differential media for the detection and enumeration of L. monocytogenes and other Listeria spp. Int. J. Food Microbiol. 8:299-316.
56. Viswanath, P., L. Murugesan, S. J. Knabel, B. Verghese, N. Chikthimmah, and L. F. La Borde. 2013. Incidence of Listeria monocytogenes and Listeria spp. in a small-scale mushroom production facility. J. Food Prot. 76:608-615.
57. Watabe, M., J. R. Rao, J. Xu, B. C. Millar, R. F. Ward, and J. E. Moore. 2004. Identification of novel eubacteria from spent mushroom compost (SMC) waste by DNA sequence typing: ecological considerations of disposal on agricultural land. Waste Manag. 24:81-86.
58. Wen, J., R. C. Anantheswaran, and S. J. Knabel. 2009. Changes in barotolerance, thermotolerance, and cellular morphology throughout the life cycle of Listeria monocytogenes. Appl. Environ. Microbiol. 75:1581-1588.
59. Wesley, I. V. 2007. Listeriosis in animals, chap. 3, p. 55-84. In E. T. Ryser and E. H. Marth (ed.), Listeria, listeriosis, and food safety. CRC Press, Boca Raton, FL.
60. Wichuk, K. M., and D. McCartney. 2007. A review of the effectiveness of current time-temperature regulations on pathogen inactivation during composting. J. Environ. Eng. Sci. 6:573-586.