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Clostridium difficile in foods and animals: history and measures to reduce exposure

  • Alex Rodriguez-Palacios (a1) (a2) (a3), Stefan Borgmann (a4) (a5), Terence R. Kline (a1) and Jeffrey T. LeJeune (a1) (a2)
Abstract

Many articles have summarized the changing epidemiology of Clostridium difficile infections (CDI) in humans, but the emerging presence of C. difficile in foods and animals and possible measures to reduce human exposure to this important pathogen have been infrequently addressed. CDIs have traditionally been assumed to be restricted to health-care settings. However, recent molecular studies indicate that this is no longer the case; animals and foods might be involved in the changing epidemiology of CDIs in humans; and genome sequencing is disproving person-to-person transmission in hospitals. Although zoonotic and foodborne transmission have not been confirmed, it is evident that susceptible people can be inadvertently exposed to C. difficile from foods, animals, or their environment. Strains of epidemic clones present in humans are common in companion and food animals, raw meats, poultry products, vegetables, and ready-to-eat foods, including salads. In order to develop science-based prevention strategies, it is critical to understand how C. difficile reaches foods and humans. This review contextualizes the current understanding of CDIs in humans, animals, and foods. Based on available information, we propose a list of educational measures that could reduce the exposure of susceptible people to C. difficile. Enhanced educational efforts and behavior change targeting medical and non-medical personnel are needed.

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*Corresponding author. E-mail: axr503@case.edu
References
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Akerlund, T, Persson, I, Unemo, M, Norén, T, Svenungsson, B, Wullt, M and Burman, LG (2008). Increased sporulation rate of epidemic Clostridium difficile Type 027/NAP1. Journal of Clinical Microbiology 46: 15301533.
al-Barrak, A, Embil, J, Dyck, B, Olekson, K, Nicoll, D, Alfa, M and Kabani, A (1999). An outbreak of toxin A negative, toxin B positive Clostridium difficile-associated diarrhea in a Canadian tertiary-care hospital. Canada Communicable Disease Report 25: 6569.
al Saif, N and Brazier, JS (1996). The distribution of Clostridium difficile in the environment of South Wales. Journal of Medical Microbiology 45: 133137.
Arroyo, LG, Kruth, SA, Willey, BM, Staempfli, HR, Low, DE and Weese, JS (2005). PCR ribotyping of Clostridium difficile isolates originating from human and animal sources. Journal of Medical Microbiology 54(Pt 2): 163166.
Arroyo, LG, Weese, JS and Staempfli, HR (2004). Experimental Clostridium difficile enterocolitis in foals. Journal of Veterinary Internal Medicine 18: 734738.
Ashiru-Oredope, D, Sharland, M, Charani, E, McNulty, C and Cooke, J (2012). Improving the quality of antibiotic prescribing in the NHS by developing a new Antimicrobial Stewardship Programme: Start Smart–Then Focus. Journal of Antimicrobial Chemotherapy 67 (Suppl. 1): i51i63.
Avbersek, J, Janezic, S, Pate, M, Rupnik, M, Zidaric, V, Logar, K, Vengust, M, Zemljic, M, Pirs, T and Ocepek, M (2009). Diversity of Clostridium difficile in pigs and other animals in Slovenia. Anaerobe 15: 252255.
Bakker, D, Corver, J, Harmanus, C, Goorhuis, A, Keessen, EC, Fawley, WN, Wilcox, MH and Kuijper, EJ (2010). Relatedness of human and animal Clostridium difficile PCR Ribotype 078 isolates determined on the basis of multilocus variable-number tandem-repeat analysis and Tetracycline resistance. Journal of Clinical Microbiology 48: 37443749.
Bakri, MM, Brown, DJ, Butcher, JP and Sutherland, AD (2009). Clostridium difficile in ready-to-eat salads, Scotland. Emerging Infectious Diseases 15: 817818.
Balassiano, IT, Yates, EA, Domingues, RM and Ferreira, EO (2012). Clostridium difficile: a problem of concern in developed countries and still a mystery in Latin America. Journal of Medical Microbiology 61: 169179.
Bandelj, P, Trilar, T, Racnik, J, Zadravec, M, Pirš, T, Avbersek, J, Micunovic, J, Ocepek, M and Vengust, M (2011). Zero prevalence of Clostridium difficile in wild passerine birds in Europe. FEMS Microbiol Letters 321: 183185.
Barbut, F, Jones, G and Eckert, C (2011). Epidemiology and control of Clostridium difficile infections in healthcare settings: an update. Current Opinion in Infectious Diseases 24: 370376.
Bartlett, JG (2008). Historical perspectives on studies of Clostridium difficile and C. difficile infection. Clinical Infectious Diseases 46 (Suppl. 1): S4S11.
Bartlett, JG, Moon, N, Chang, TW, Taylor, N and Onderdonk, AB (1978). Role of Clostridium difficile in antibiotic-associated pseudomembranous colitis. Gastroenterology 75: 778782.
Bauer, MP, Notermans, DW, van Benthem, VHB, Brazier, JS, Wilcox, M, Rupnik, M, Monnet, D, van Dissel, JT, Kuijper, EJ, ECDIS Study Group (2011). Clostridium difficile, infection in Europe: a hospital-based survey. The Lancet 377: 6373.
Baverud, V (2004). Clostridium difficile diarrhea: infection control in horses. Veterinary Clinics of North America Equine Practice 20: 615630.
Baverud, V, Gustafsson, A, Franklin, A, Aspan, A and Gunnarsson, A (2003). Clostridium difficile: prevalence in horses and environment, and antimicrobial susceptibility. Equine Veterinary Journal 35: 465471.
Bongaerts, GPA and Lyerly, DM (1997). Role of bacterial metabolism and physiology in the pathogenesis of Clostridium difficile disease. Microbial Pathogenesis 22: 253256.
Borgmann, S, Kist, M, Jakobiak, T, Reil, M, Scholz, E, von Eichel-Streiber, C, Gruber, H, Brazier, JS and Schulte, B (2008). Increased number of Clostridium difficile infections and prevalence of Clostridium difficile PCR ribotype 001 in southern Germany. Euro Surveillance 13: pii = 19057. [Available online at http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19057]. Last accessed November 19, 2012.
Borriello, SP, Honour, P and Barclay, F (1983a). Foodborne transmission of Clostridium difficile. Gastroenterology 84: 201.
Borriello, SP, Honour, P, Turner, T and Barclay, F (1983b). Household pets as a potential reservoir for Clostridium difficile infection. Journal of Clinical Pathology 36: 8487.
Broda, DM, DeLacy, KM, Bell, RG, Braggins, TJ and Cook, RL (1996). Psychrotrophic Clostridium spp. associated with ‘blown pack’ spoilage of chilled vacuum-packed red meats and dog rolls in gas-impermeable plastic casings. International Journal of Food Microbiology 29: 335352.
Burckhardt, F, Friedrich, A, Beier, D and Eckmanns, T (2008). Clostridium difficile surveillance trends, Saxony, Germany. Emerging Infectious Diseases 14: 691692.
CFIA (2010). Canadian Food Inspection Agency. Food Thermometer Food Safety Tips: Preventing foodborne Illness. [Available online at http://www.inspection.gc.ca/english/fssa/concen/tipcon/thermoe.shtml]. Last accessed November 19, 2012.
Chomel, BB and Sun, B (2011). Zoonoses in the bedroom. Emerging Infectious Diseases 17: 167172.
Clements, AC, Magalhaes, RJ, Tatem, AJ, Paterson, DL and Riley, TV (2010). Clostridium difficile PCR ribotype 027: assessing the risks of further worldwide spread. Lancet Infectious Diseases 10: 395404.
Cohen, SH, Gerding, DN, Johnson, S, Kelly, CP, Loo, VG, McDonald, LC, Pepin, J and Wilcox, MH (2010). Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the society for healthcare epidemiology of America (SHEA) and the infection diseases society of America (IDSA). Infection Control Hospital Epidemiology 31: 4314355.
Costa, MC, Stampfli, HR, Arroyo, LG, Pearl, DL and Weese, JS (2011). Epidemiology of Clostridium difficile on a veal farm: prevalence, molecular characterization and tetracycline resistance. Veterinary Microbiology 152: 379384.
Curry, SR, Marsh, JW, Schlackman, JL and Harrison, LH (2012). Prevalence of Clostridium difficile in uncooked ground meat products from Pittsburgh, Pennsylvania. Applied and Environmental Microbiology 78: 41834186.
Debast, SB, van Leengoed, LA, Goorhuis, A, Harmanus, C, Kuijper, EJ and Bergwerff, AA (2009). Clostridium difficile PCR ribotype 078 toxinotype V found in diarrhoeal pigs identical to isolates from affected humans. Environmental Microbiology 11: 505511.
Deneve, C, Delomenie, C, Barc, M-C, Collignon, A and Janoir, C (2008). Antibiotics involved in Clostridium difficile-associated disease increase colonization factor gene expression. Journal of Medical Microbiology 57: 732738.
Dubberke, ER and Wertheimer, AI (2009). Review of current literature on the economic burden of Clostridium difficile infection. Infection Control Hospital Epidemiology 30: 5766.
Ehrich, M, Perry, BD, Troutt, HF, Dellers, RW and Magnusson, RA (1984). Acute diarrhea in horses of the Potomac River area: examination for clostridial toxins. Journal of the American Veterinary Medical Association 185: 433435.
Enoch, DA, Butler, MJ, Pai, S, Aliyu, SH and Karas, JA (2011). Clostridium difficile in children: colonisation and disease. Journal of Infection 63: 105113.
Eyre, DW, Golubchik, T, Gordon, NC, Bowden, R, Piazza, P, Batty, EM, Ip, CL, Wilson, DJ, Didelot, X, O'Connor, L, Lay, R, Buck, D, Kearns, AM, Shaw, A, Paul, J, Wilcox, MH, Donnelly, PJ, Peto, TE, Walker, AS and Crook, DW (2012). A pilot study of rapid benchtop sequencing of Staphylococcus aureus and Clostridium difficile for outbreak detection and surveillance. BMJ Open 2: pii: e001124.
Faires, MC, Pearl, DL, Ciccotelli, WA, Straus, K, Zinken, G, Berke, O, Reid-Smith, RJ and Weese, JS (2012). A prospective study to examine the epidemiology of methicillin-resistant Staphylococcus aureus and Clostridium difficile contamination in the general environment of three community hospitals in southern Ontario, Canada. BMC Infectious Diseases 12: 290.
Finley, R, Reid-Smith, R and Weese, JS (2006). Human health implications of Salmonella-contaminated natural pet treats and raw pet food. Clinical Infectious Diseases 42: 686691.
Forgetta, V, Oughton, MT, Marquis, P, Brukner, I, Blanchette, R, Haub, K, Magrini, V, Mardis, ER, Gerding, DN, Loo, VG, Miller, MA, Mulvey, MR, Rupnik, M, Dascal, A and Dewar, K (2011). Fourteen-genome comparison identifies DNA markers for severe-disease-associated strains of Clostridium difficile. Journal of Clinical Microbiology 49: 22302238.
Freeman, J, Bauer, MP, Baines, SD, Corver, J, Fawley, WN, Goorhuis, B, Kuijper, EJ and Wilcox, MH (2010). The changing epidemiology of Clostridium difficile infections. Clinical Microbiology Reviews 23: 529549.
French, E, Rodriguez-Palacios, A and LeJeune, JT (2010). Enteric bacterial pathogens with zoonotic potential isolated from farm-raised deer. Foodborne Pathogens and Disease 7: 10311037.
George, RH, Symonds, JM, Dimock, F, Brown, JD, Arabi, Y, Shinagawa, N, Keighley, MR, Alexander-Williams, J and Burdon, DW (1978). Identification of Clostridium difficile as a cause of pseudomembranous colitis. British Medical Journal 1: 695.
Gerding, DN, Muto, CA and Owens, RC (2008). Measures to control and prevent Clostridium difficile infection. Clinical Infectious Diseases 46 (Suppl 1): S43S49.
Geric, B, Carman, RJ, Rupnik, M, Genheimer, CW, Sambol, SP, Lyerly, DM, Gerding, DN and Johnson, S (2006). Binary toxin-producing, large clostridial toxin-negative Clostridium difficile strains are enterotoxic but do not cause disease in hamsters. Journal of Infectious Disease 193: 11431150.
Geric, B, Rupnik, M, Gerding, DN, Grabnar, M and Johnson, S (2004). Distribution of Clostridium difficile variant toxinotypes and strains with binary toxin genes among clinical isolates in an American hospital. Journal of Medical Microbiology 53(Pt 9): 887994.
Ghantoji, SS, Sail, K, Lairson, DR, DuPont, HL and Garey, KW (2010). Economic healthcare costs of Clostridium difficile infection: a systematic review. Journal of Hospital Infection 74: 309318.
Goodhand, JR, Alazawi, W and Rampton, DS (2011). Systematic review: Clostridium difficile and inflammatory bowel disease. Alimentary Pharmacology and Therapeutics 33: 428441.
Goorhuis, A, Bakker, D, Corver, J, Debast, SB, Harmanus, C, Notermans, DW, Bergwerff, AA, Dekker, FW and Kuijper, EJ (2008). Emergence of Clostridium difficile infection due to a new hypervirulent strain, polymerase chain reaction ribotype 078. Clinical Infectious Diseases 47: 11621170.
Gould, LH and Limbago, B (2010). Clostridium difficile in food and domestic animals: a new foodborne pathogen? Clinical Infectious Diseases 51: 577582.
Gurian, L, Ward, TT and Katon, RM (1982). Possible foodborne transmission in a case of pseudomembranous colitis due to Clostridium difficile: influence of gastrointestinal secretions on Clostridium difficile infection. Gastroenterology 83: 465469.
Hamm, EE, Voth, DE and Ballard, JD (2006). Identification of Clostridium difficile toxin B cardiotoxicity using a zebrafish embryo model of intoxication. Proceedings of the National Academy of SciencesUSA 103: 1417614181.
Hammitt, MC, Bueschel, DM, Keel, MK, Glock, RD, Cuneo, P, DeYoung, DW, Reggiardo, C, Trinh, HT and Songer, JG (2008). A possible role for Clostridium difficile in the etiology of calf enteritis. Veterinary Microbiology 127: 343352.
Harvey, RB, Norman, KN, Andrews, K, Hume, ME, Scanlan, CM, Callaway, TR, Anderson, RC, and Nisbet, DJ (2011). Clostridium difficile in poultry and poultry meat. Foodborne Pathogens and Diseases 8: 13211323.
He, M, Miyajima, F, Roberts, P, Parkhill, J and Lawley, TD (2012). Emergence and global spread of epidemic healthcare-associated Clostridium difficile. Nature Genetics 45: 109113.
He, M, Sebaihia, M, Lawley, TD, Stabler, RA, Dawson, LF, Martin, MJ, Holt, KE, Seth-Smith, HM, Quail, MA, Rance, R, Brooks, K, Churcher, C, Harris, D, Bentley, SD, Burrows, C, Clark, L, Corton, C, Murray, V, Rose, G, Thurston, S, van Tonder, A, Walker, D, Wren, BW, Dougan, G and Parkhill, J (2010). Evolutionary dynamics of Clostridium difficile over short and long time scales. Proceedings of the National Academy of Sciences USA 107: 75277532.
Hell, M, Permoser, M, Chmelizek, G, Kern, J, Maass, M, Huhulescu, S, Indra, A and Allerberger, F (2011). Clostridium difficile infection: monoclonal or polyclonal genesis? Infection 39: 4614665.
Hensgens, MP, Goorhuis, A, Notermans, DW, van Benthem, BH and Kuijper, EJ (2009). Decrease of hypervirulent Clostridium difficile PCR ribotype 027 in the Netherlands. European Surveillance 14: pii: 19402.
Hensgens, MP, Keessen, EC, Squire, MM, Riley, TV, Koene, MG, de Boer, E, Lipman, LJ and Kuijper, EJ (2012). Clostridium difficile infection in the community: a zoonotic disease? Clinical Microbiology and Infection 18: 635645.
Hensgens, M, van Dorp, SM, Harmanus, C, Sanders, I, Corver, J, Kuijper, EJ, Notermans, DW, Benthem, V, Alblas, J and Coutinho, R, (2012). Sixth annual report of the National Reference Laboratory for Clostridium difficile (May 2011 to May 2012) and results of the sentinel surveillance. Available from http://www.rivm.nl/Zoeken?query=difficile+report
Hensgens, M, Harmanus, C, Sanders, I, Corver, J, Kuijper, EJ, Notermans, DW, Benthem, V, Alblas, J and Coutinho, R, (2011). Fifth annual report of the National Reference Laboratory for Clostridium difficile (May 2010 to May 2011) and results of the sentinel surveillance. Available from: http://www.rivm.nl/Zoeken?query=difficile+report
Hirshon, J, Thompson, A, Limbago, B, McDonald, L, Bonkosky, M, Heimer, R, Meek, J, Mai, V and Braden, C (2011). Clostridium difficile infection in outpatients, Maryland and Connecticut, USA, 2002–2007. Emerging Infectious Diseases 17: 19461949.
Houser, BA, Soehnlen, MK, Wolfgang, DR, Lysczek, HR, Burns, CM, Jayarao, BM (2012). Prevalence of Clostridium difficile toxin genes in the feces of veal calves and incidence of ground veal contamination. Foodborne Pathogens and Diseases 9: 3236.
Huang, H, Wu, S, Wang, M, Zhang, Y, Fang, H, Palmgren, AC, Weintraub, A and Nord, CE (2008). Molecular and clinical characteristics of Clostridium difficile infection in a University Hospital in Shanghai, China. Clinical Infectious Diseases 47: 16061608.
Hurley, BW and Nguyen, CC (2002). The spectrum of pseudomembranous enterocolitis and antibiotic-associated diarrhea. Archives of Internal Medicine 162: 21772184.
I.G.H.A./HorseAid's U.S.D.A. Report (1997) U.S.D.A. Promotes Horse & Goat Meat. [Available online at http://www.igha.org/USDA.html]. Last accessed November 19, 2012.
Indra, A, Lassnig, H, Baliko, N, Much, P, Fiedler, A, Huhulescu, S and Allerberger, F (2009). Clostridium difficile: a new zoonotic agent? Wien Klin Wochenschr 121: 9195.
Janezic, S, Ocepek, M, Zidaric, V and Rupnik, M (2012). Clostridium difficile genotypes other than ribotype 078 that are prevalent among human, animal and environmental isolates. BMC Microbiology 12: 48.
Janvilisri, T, Scaria, J, Thompson, AD, Nicholson, A, Limbago, BM, Arroyo, LG, Songer, JG, Grohn, YT and Chang, YF (2009). Microarray identification of Clostridium difficile core components and divergent regions associated with host origin. Journal of Bacteriology 191: 38813891.
Jin, K, Wang, S, Zhang, C, Xiao, Y, Lu, S and Huang, Z (2013). Protective antibody responses against Clostridium difficile elicited by a DNA vaccine expressing the enzymatic domain of toxin B. Human Vaccine Immunotherapy 9(1): [Epub ahead of print. PMID: 23143772, available at: http://dx.doi.org/10.4161/hv.22434]
Jones, MA and Hunter, D (1983). Isolation of Clostridium difficile from pigs. Veterinary Record 112: 253.
Kaatz, GW, Gitlin, SD, Schaberg, DR, Wilson, KH, Kauffman, CA, Seo, SM and Fekety, R (1988). Acquisition of Clostridium difficile from the hospital environment. American Journal of Epidemiology 127: 12891294.
Keel, K, Brazier, JS, Post, KW, Weese, S and Songer, JG (2007). Prevalence of PCR ribotypes among Clostridium difficile isolates from pigs, calves, and other species. Journal of Clinical Microbiology 45: 19631964.
Keel, MK and Songer, JG (2007). The distribution and density of Clostridium difficile toxin receptors on the intestinal mucosa of neonatal pigs. Veterinary Pathology 44: 814822.
Keel, MK and Songer, JG (2011). The attachment, internalization, and time-dependent, intracellular distribution of Clostridium difficile toxin A in porcine intestinal explants. Veterinary Pathology Online 48: 369380.
Keessen, EC, van den Berkt, AJ, Haasjes, NH, Hermanus, C, Kuijper, CE and Lipman, LJ (2011). The relation between farm specific factors and prevalence of Clostridium difficile in slaughter pigs. Veterinary Microbiology 154: 130134.
Kelly, CP and Kyne, L (2011). The host immune response to Clostridium difficile. Journal of Medical Microbiology 60(Pt 8): 10701079.
Kelly, CP and LaMont, JT (2008). Clostridium difficile – more difficult than ever. New England Journal of Medicine 359: 19321940.
Kho Sugeng, C (2012). Determining the growth limiting conditions and prevalence of Clostridium difficile in foods. MSc Thesis. University of Ottawa, Canada.
Kim, H, Riley, TV, Kim, M, Kim, CK, Yong, D, Lee, K, Chong, Y and Park, JW (2008). Increasing prevalence of toxin A-negative, toxin B-positive isolates of Clostridium difficile in Korea: impact on laboratory diagnosis. Journal of Clinical Microbiology 46: 11161117.
Kiss, D and Bilkei, G (2005). A new periparturient disease in Eastern Europe, Clostridium difficile causes postparturient sow losses. Theriogenology 63: 1723.
Koene, MG, Mevius, D, Wagenaar, JA, Harmanus, C, Hensgens, MP, Meetsma, AM, Putirulan, FF, van Bergen, MA and Kuijper, EJ (2012). Clostridium difficile in Dutch animals: their presence, characteristics and similarities with human isolates. Clinical Microbiology and Infection 18: 778784.
Kuehne, SA, Cartman, ST, Heap, JT, Kelly, ML, Cockayne, A and Minton, NP (2010). The role of toxin A and toxin B in Clostridium difficile infection. Nature 467: 711713.
Kuijper, EJ and van Dissel, JT (2008). Spectrum of Clostridium difficile infections outside health care facilities. Canadian Medical Association Journal 179: 747748.
Kuijper, EJ, Barbut, F, Brazier, JS, Kleinkauf, N, Eckmanns, T, Lambert, ML, Drudy, D, Fitzpatrick, F, Wiuff, C, Brown, DJ, Coia, JE, Pituch, H, Reichert, P, Even, J, Mossong, J, Widmer, AF, Olsen, KE, Allerberger, F, Notermans, DW, Delmée, M, Coignard, B, Wilcox, M, Patel, B, Frei, R, Nagy, E, Bouza, E, Marin, M, Åkerlund, T, Virolainen-Julkunen, A, Lyytikäinen, O, Kotila, S, Ingebretsen, A, Smyth, B, Rooney, P, Poxton, IR, Monnet, DL. Update of Clostridium difficile infection due to PCR ribotype 027 in Europe, 2008. Euro Surveill. 2008;13(31):pii=18942. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=18942
Lanis, JM, Hightower, LD, Shen, A and Ballard, JD (2012). TcdB from hypervirulent Clostridium difficile exhibits increased efficiency of autoprocessing. Molecular Microbiology 84: 6676.
Larson, HE, Price, AB, Honour, P and Borriello, SP (1978). Clostridium difficile and the aetiology of pseudomembranous colitis. Lancet 1: 10631066.
Lawley, TD, Clare, S, Walker, AW, Goulding, D, Stabler, RA, Croucher, N, Mastroeni, P, Scott, P, Raisen, C, Mottram, L, Fairweather, NF, Wren, BW, Parkhill, J and Dougan, G (2009). Antibiotic treatment of Clostridium difficile carrier mice triggers a supershedder state, spore-mediated transmission, and severe disease in immunocompromised hosts. Infection and Immunity 77: 36613669.
Lefebvre, SL, Arroyo, LG and Weese, JS (2006). Epidemic Clostridium difficile strain in hospital visitation dog. Emerging Infectious Diseases 12: 10361037.
Legaria, MC, Lumelsky, G and Rosetti, S (2003). ARGENTINA Clostridium difficile-associated diarrhea from a general hospital in Argentina. Anaerobe 9: 113116.
Lengacher, B, Kline, TR, Harpster, L, Williams, ML and Lejeune, JT (2011). Low prevalence of Escherichia coli O157:H7 in horses in Ohio, USA. Journal of Food Protection 73: 20892092.
Lessa, FC, Gould, CV and McDonald, LC (2012). Current status of Clostridium difficile infection epidemiology. Clinical Infectious Diseases 55 (suppl. 2): S6570.
Lim, PL, Ling, ML, Lee, HY, Koh, TH, Tan, AL, Kuijper, EJ, Goh, SS, Low, BS, Ang, LP, Harmanus, C, Lin, RTP, Krishnan, P, James, L and Lee, CE (2011). Isolation of the first three cases of Clostridium difficile polymerase chain reaction ribotype 027 in Singapore. Singapore Medical Journal 5: 361364.
Limbago, B, Thompson, AD, Greene, SA, MacCannell, D, MacGowan, CE, Jolbitado, B, Hardin, HD, Estes, SR, Weese, JS, Songer, JG and Gould, LH (2012). Development of a consensus method for culture of Clostridium difficile from meat and its use in a survey of U.S. retail meats. Food Microbiology 32: 448451.
Linsky, A, Gupta, K, Lawler, EV, Fonda, JR and Hermos, JA (2010). Proton pump inhibitors and risk for recurrent Clostridium difficile infection. Archives of Internal Medicine 170: 772778.
Loo, VG, Poirier, L, Miller, MA, Oughton, M, Libman, MD, Michaud, S, Bourgault, AM, Nguyen, T, Frenette, C, Kelly, M, Vibien, A, Brassard, P, Fenn, S, Dewar, K, Hudson, TJ, Horn, R, Rene, P, Monczak, Y and Dascal, A (2005). A predominantly clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. New England Journal of Medicine 353: 24422449.
Lyras, D, O'Connor, JR, Howarth, PM, Sambol, SP, Carter, GP, Phumoonna, T, Poon, R, Adams, V, Vedantam, G, Johnson, S, Gerding, DN and Rood, JI (2009). Toxin B is essential for virulence of Clostridium difficile. Nature 458: 11761179.
Marler, B. (2010). About Clostridium difficile. Food Poison Journal – Food Poisoning Outbreaks and Litigation: Surveillance and analysis. [Available online at http://www.foodpoisonjournal.com/food-poisoning-information/about-clostridium-difficile/]. Last accessed November 19, 2012.
Marsh, JW, Tulenko, MM, Shutt, KA, Thompson, AD, Weese, JS, Songer, JG, Limbago, BM and Harrison, LH (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: 156160.
Mazuski, JE, Panesar, N, Tolman, K and Longo, WE (1998). In Vitro Effects of Clostridium difficileToxins on Hepatocytes. The Journal of Surgical Research 79: 170178.
McFarland, LV (2008). Update on the changing epidemiology of Clostridium difficile-associated disease. Nature Clinical Practice Gastroenterology and Hepatology 5: 4048.
Medina-Torres, CE, Weese, JS and Staempfli, HR (2011). Prevalence of Clostridium difficile in horses. Veterinary Microbiology 152: 212215.
Meisel-Mikolajczyk, F, Kaliszuk-Kaminska, E and Martirosian, G (1995). Study of the thermoresistance of Clostridium difficile spores. Medycyna Doswiadczalna I Mikrobiologia (Warszawa) 47: 177181.
Metcalf, D, Avery, BP, Janecko, N, Matic, N, Reid-Smith, R and Weese, JS (2011). Clostridium difficile in seafood and fish. Anaerobe 17: 8586.
Metcalf, DS, Costa, MC, Dew, WM and Weese, JS (2010). Clostridium difficile in vegetables, Canada. Letters in Applied Microbiology 51: 600602.
Modi, N, Gulati, N, Solomon, K, Monaghan, T, Robins, A, Sewell, HF and Mahida, YR (2011). Differential binding and internalization of Clostridium difficile toxin A by human peripheral blood monocytes, neutrophils and lymphocytes. Scandinavian Journal of Immunology 74: 264271.
Montgomery, SP, Xiao, L and Cama, V (2011). Comment on zoonoses in the bedroom. Emerging Infectious Diseases 17: 1340; author reply 1341.
Moran, L, Scates, P and Madden, RH (2009). Prevalence of Campylobacter spp. in raw retail poultry on sale in Northern Ireland. Journal of Food Protection 72: 18301835.
Mulvey, MR, Boyd, DA, Gravel, D, Hutchinson, J, Kelly, S, McGeer, A, Moore, D, Simor, A, Suh, KN, Taylor, G, Weese, JS and Miller, M (2010). Hypervirulent Clostridium difficile strains in hospitalized patients, Canada. Emerging Infectious Diseases 16: 678681.
Naumova, EN, Jagai, JS, Matyas, B, DeMaria, A Jr, MacNeill, IB and Griffiths, JK (2007). Seasonality in six enterically transmitted diseases and ambient temperature. Epidemiology and Infection 135: 281292.
Noren, T, Akerlund, T, Back, E, Sjoberg, L, Persson, I, Alriksson, I and Burman, LG (2004). Molecular epidemiology of hospital-associated and community-acquired Clostridium difficile infection in a Swedish county. Journal of Clinical Microbiology 42: 36353643.
Norman, KN, Harvey, RB, Scott, HM, Hume, ME, Andrews, K and Brawley, AD (2009). Varied prevalence of Clostridium difficile in an integrated swine operation. Anaerobe 15: 256260.
Nylund, CM, Goudie, A, Garza, JM, Fairbrother, G and Cohen, MB (2011). Clostridium difficile infection in hospitalized children in the United States. Archives of Pediatric and Adolescent Medicine 165: 451457.
O'Brien, JA, Lahue, BJ, Caro, JJ and Davidson, DM (2007). The emerging infectious challenge of Clostridium difficile-associated disease in Massachusetts hospitals: clinical and economic consequences. Infection Control and Hospital Epidemiology 28: 12191227.
Onwueme, K, Fadairo, Y, Idoko, L, Onuh, J, Alao, O, Agaba, P, Lawson, L, Ukomadu, C and Idoko, J (2011). High prevalence of toxinogenic Clostridium difficile in Nigerian adult HIV patients. Transactions of the Royal Society of Tropical Medicine and Hygiene 105: 667669.
Pasquale, V, Romano, V, Rupnik, M, Capuano, F, Bove, D, Aliberti, F, Krovacek, K and Dumontet, S, (2012). Occurance of toxigenic Clostridium difficile in edible bivalve molluscs. Food Microbiology 31: 309312.
Pawar, D, Tsay, R, Nelson, DS, Elumalai, MK, Lessa, FC, Clifford McDonald, L and Dumyati, G (2012). Burden of Clostridium difficile infection in long-term care facilities in Monroe County, New York. Infection Control and Hospital Epidemiology 33: 11071112.
Pell, AN (1997). Manure and microbes: public and animal health problem? Journal of Dairy Science 80: 26732681.
Pepin, J, Alary, ME, Valiquette, L, Raiche, E, Ruel, J, Fulop, K, Godin, D and Bourassa, C (2005). Increasing risk of relapse after treatment of Clostridium difficile colitis in Quebec, Canada. Clinical Infectious Diseases 40: 15911597.
Pepin, J, Valiquette, L, Alary, ME, Villemure, P, Pelletier, A, Forget, K, Pepin, K and Chouinard, D (2004). Clostridium difficile-associated diarrhea in a region of Quebec from 1991 to 2003: a changing pattern of disease severity. Canadian Medical Association Journal 171: 466472.
Polgreen, P, Yang, M, Lucas, M, Bohnett, M and Cavanaugh, J (2010). A time-series analysis of Clostridium difficile and its seasonal association with Influenza. Infection Control and Hospital Epidemiology 31: 382387.
Porter, MC, Reggiardo, C, Glock, RD, Keel, MK and Songer, JG (2002). Association of Clostridium difficile with bovine neonatal diarrhea [abstract]. In: Abstracts of the Proceedings of the American Association of Veterinary Laboratory Diagosticians. 45th Annual Meeting. St. Louis, Missouri; 2002 19–21 October. American Association of Veterinary Laboratory Diagosticians, Davis, CA, USA.
Post, KW, Jost, BH and Songer, JG (2002). Evaluation of a test for Clostridium difficile toxins A and B for the diagnosis of neonatal swine enteritis. Journal of Veterinary Diagnostic Investigations 14: 258259.
Price, AB and Davies, DR (1977). Pseudomembranous colitis. Journal of Clinical Pathology 30: 112.
Quesada-Gomez, C, Mulvey, M, Vargas, P, Gamboa-Coronadom, MM, Rodriguez-Cavallini, E and Rodriguez, C (2013). Isolation of a toxigenic and clinical genotype of Clostridium difficile in retail meats in Costa Rica. Journal of Food Protection 76: DOI 10.4315/0362-028X.JFP-12-169.
Reil, M, Erhard, M, Kuijper, EJ, Kist, M, Zaiss, H, Witte, W, Gruber, H and Borgmann, S (2011). Recognition of Clostridium difficile PCR-ribotypes 001, 027 and 126/078 using an extended MALDI-TOF MS system. European Journal of Clinical Microbiology and Infectious Disease 30: 14311436.
Reil, M, Hensgens, MP, Kuijper, EJ, Jakobiak, T, Gruber, H, Kist, M and Borgmann, S (2012). Seasonality of Clostridium difficile infections in Southern Germany. Epidemiology and Infection 140: 17871793.
Riley, TV (1998). Clostridium difficile: a pathogen of the nineties. European Journal of Clinical Microbiology and Infectious Disease 17: 137141.
Roberts, K, Smith, CF, Snelling, AM, Kerr, KG, Banfield, KR, Sleigh, PA and Beggs, CB (2008). Aerial dissemination of Clostridium difficile spores. BMC Infectious Disease 8: 7.
Rodriguez-Palacios, A (2011). Ecology and epidemiology of human pathogen Clostridium difficile in foods, food animals and wildlife. PhD Thesis. The Ohio State University, Wooster, Ohio,USA.
Rodriguez-Palacios, A and LeJeune, JT (2011). Moist-heat resistance, spore aging, and superdormancy in Clostridium difficile. Applied and Environmental Microbiology 77: 30853091.
Rodriguez-Palacios, A, Koohmaraie, M and LeJeune, JT (2011a). Prevalence, enumeration, and antimicrobial agent resistance in Clostridium difficile in cattle at harvest in the United States. Journal of Food Protection 74: 16181624.
Rodriguez-Palacios, A, LeJeune, JT and Hoover, DG (2012). Clostridium difficile: an emerging food safety risk. Food Technology, Chicago 66: 40. [Available online at: http://cfaes.osu.edu/sites/cfaes_main/files/site-library/site-documents/News/C_diff_an_Emerging_Food_Safety_Risk.pdf]. Last accessed November 21, 2012.
Rodriguez-Palacios, A, Pickworth, C, Loerch, S and Lejeune, JT (2011b). Transient fecal shedding and limited animal-to-animal transmission of Clostridium difficile by naturally infected finishing feedlot cattle. Applied and Environmental Microbiology 77: 33913397.
Rodriguez-Palacios, A, Reid-Smith, RJ, Staempfli, HR, Daignault, D, Janecko, N, Avery, BP, Martin, H, Thomspon, AD, McDonald, LC, Limbago, B and Weese, JS (2009). Possible seasonality of Clostridium difficile in retail meat, Canada. Emerging Infectious Diseases 15: 802805.
Rodriguez-Palacios, A, Reid-Smith, RJ, Staempfli, HR and Weese, JS (2010). Clostridium difficile survives minimal temperature recommended for cooking ground meats. Anaerobe 16: 540542.
Rodriguez-Palacios, A, Stampfli, HR, Duffield, T, Peregrine, AS, Trotz-Williams, LA, Arroyo, LG, Brazier, JS and Weese, JS (2006). Clostridium difficile PCR ribotypes in calves, Canada. Emerging Infectious Diseases 12: 17301736.
Rodriguez-Palacios, A, Staempfli, HR, Duffield, T and Weese, JS (2007a). Clostridium difficile in retail ground meat, Canada. Emerging Infectious Diseases 13: 485487.
Rodriguez-Palacios, A, Stampfli, HR, Stalker, M, Duffield, T and Weese, JS (2007b). Natural and experimental infection of neonatal calves with Clostridium difficile. Veterinary Microbiology 124: 166172.
Rodriguez, C, Taminiau, B, Van Broeck, J, Avesani, V, Delmee, M and Daube, G (2012). Clostridium difficile in young farm animals and slaughter animals in Belgium. Anaerobe pii: S1075-9964(12)00141-2 18: 621625.
Rupnik, M (2007). Is Clostridium difficile-associated infection a potentially zoonotic and foodborne disease? Clinical Microbiology and Infection 13: 457459.
Rupnik, M, Dupuy, B, Fairweather, NF, Gerding, DN, Johnson, S, Just, I, Lyerly, DM, Popoff, MR, Rood, JI, Sonenshein, AL, Thelestam, M, Wren, BW, Wilkins, TD and von Eichel-Streiber, C (2005). Revised nomenclature of Clostridium difficile toxins and associated genes. Journal of Medical Microbiology 54(Pt 2): 113117.
Rupnik, M, Kato, N, Grabnar, M and Kato, H (2003). New types of toxin A-negative, toxin B-positive strains among Clostridium difficile isolates from Asia. Journal of Clinical Microbiology 41: 11181125.
Rupnik, M, Widmer, A, Zimmermann, O, Eckert, C and Barbut, F (2008). Clostridium difficile toxinotype V, ribotype 078, in animals and humans. Journal of Clinical Microbiology 46: 2146.
Rupnik, M, Wilcox, MH and Gerding, DN (2009). Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nature Reviews Microbiology 7: 526536.
Sailhamer, EA, Carson, K, Chang, Y, Zacharias, N, Spaniolas, K, Tabbara, M, Alam, HB, DeMoya, MA and Velmahos, GC (2009). Fulminant Clostridium difficile colitis: patterns of care and predictors of mortality. Archives of Surgery 144: 433440.
Sawabe, E, Kato, H, Osawa, K, Chida, T, Tojo, N, Arakawa, Y and Okamura, N (2007). JAPAN first 027 – molecular analysis of Clostridium difficile at a university teaching hospital in Japan: a shift in the predominant type over a five-year period. European Journal of Clinical Microbiology and Infectious Diseases 26: 695703.
Scallan, E, Hoekstra, RM, Angulo, FJ, Tauxe, RV, Widdowson, MA, Roy, SL, Jones, JL and Griffin, PM (2011). Foodborne illness acquired in the United States – major pathogens. Emerging Infectious Diseases 17: 715.
Scaria, J, Janvilisri, T, Fubini, S, Gleed, RD, McDonough, SP and Chang, Y-F (2011). Clostridium difficile transcriptome analysis using pig ligated loop model reveals modulation of pathways not modulated in vitro. Journal of Infectious Diseases 203: 16131620.
Schwan, C, Stecher, BR, Tzivelekidis, T, van Ham, M, Rohde, M, Hardt, WD, Wehland, JR and Aktories, K (2009). Clostridium difficile toxin CDT induces formation of microtubule-based protrusions and increases adherence of bacteria. PLoS Pathogens 5: e1000626.
Shin, BM, Kuak, EY, Yoo, HM, Kim, EC, Lee, K, Kang, JO, Whang, DH and Shin, JH (2008a). Multicentre study of the prevalence of toxigenic Clostridium difficile in Korea: results of a retrospective study 2000–2005. Journal of Medical Microbiology 57(Pt 6): 697701.
Shin, BM, Kuak, EY, Yoo, SJ, Shin, WC and Yoo, HM (2008b). Emerging toxin AB+ variant strain of Clostridium difficile responsible for pseudomembranous colitis at a tertiary care hospital in Korea. Diagnostic Microbiology and Infectious Disease 60: 333337.
Simango, C (2006). Prevalence of Clostridium difficile in the environment in a rural community in Zimbabwe. Transactions of the Royal Society of Tropical Medicine and Hygiene 100: 11461150.
Simango, C and Mwakurudza, S (2008). Clostridium difficile in broiler chickens sold at market places in Zimbabwe and their antimicrobial susceptibility. International Journal of Food Microbiology 124: 268270.
Sinh, P, Barrett, TA and Yun, L (2011). Clostridium difficile infection and inflammatory bowel disease: a review. Gastroenterology Research and Practice 2011: 11.
Smith, LD and King, EO (1962). Occurrence of Clostridium difficile in infections of man. Journal of Bacteriology 84: 6567.
Songer, JG (2004). The emergence of Clostridium difficile as a pathogen of food animals. Animal Health Research Reviews 5: 321326.
Songer, JG (2010). Clostridia as agents of zoonotic disease. Veterinary Microbiology 140: 399404.
Songer, JG, Trinh, HT, Dial, SM, Brazier, JS and Glock, RD (2009). Equine colitis X associated with infection by Clostridium difficile NAP1/027. Journal of Veterinary Diagnostic Investigation 21: 377380.
Spigaglia, P, Barbanti, F, Mastrantonio, P, Brazier, JS, Barbut, F, Delmee, M, Kuijper, E and Poxton, IR (2008). Fluoroquinolone resistance in Clostridium difficile isolates from a prospective study of C. difficile infections in Europe . Journal of Medical Microbiology 57(Pt 6): 784789.
Stabler, RA, Gerding, DN, Songer, JG, Drudy, D, Brazier, JS, Trinh, HT, Witney, AA, Hinds, J and Wren, BW (2006). Comparative phylogenomics of Clostridium difficile reveals clade specificity and microevolution of hypervirulent strains. Journal of Bacteriology 188: 72977305.
Stare, BG, Delmee, M and Rupnik, M (2007). Variant forms of the binary toxin CDT locus and tcdC gene in Clostridium difficile strains. Journal of Medical Microbiology 56(Pt 3): 329335.
Steele, J, Feng, H, Parry, N and Tzipori, S (2010). Piglet models of acute or chronic Clostridium difficile illness. Journal of Infectious Diseases 201: 428434.
Steer, HW (1975). The pseudomembranous colitis associated with clindamycin therapy – a viral colitis. Gut 16: 695706.
Sun, X, Savidge, T and Feng, H (2010). The enterotoxicity of Clostridium difficile toxins. Toxins 2: 18481880.
Susick, EK, Putnam, M, Bermudez, DM and Thakur, S (2012). Longitudinal study comparing the dynamics of Clostridium difficile in conventional and antimicrobial free pigs at farm and slaughter. Veterinary Microbiology. 157: 172178.
Tae, CH, Jung, SA, Song, HJ, Kim, SE, Choi, HJ, Lee, M, Hwang, Y, Kim, H and Lee, K (2009). The first case of antibiotic-associated colitis by Clostridium difficile PCR ribotype 027 in Korea. Journal of Korean Medical Science 24: 520524.
Tedesco, FJ, Stanley, RJ and Alpers, DH (1974). Diagnostic features of clindamycin-associated pseudomembranous colitis. New England Journal of Medicine 290: 841843.
Terhes, G, Urban, E, Soki, J, Hamid, KA and Nagy, E (2004). Community-Acquired Clostridium difficile Diarrhea Caused by Binary Toxin, Toxin A, and Toxin B Gene-Positive Isolates in Hungary. Journal of Clinical Microbiology 42: 43164318.
Thakur, S, Sandfoss, M, Kennedy-Stoskopf, S and Deperno, CS (2011). Detection of Clostridium difficile and Salmonella in feral swine population in North Carolina. Journal of Wildlife Diseases 47: 774776.
Thitaram, SN, Frank, JF, Lyon, SA, Siragusa, GR, Bailey, JS, Lombard, JE, Haley, CA, Wagner, BA, Dargatz, DA and Fedorka-Cray, PJ (2011). Clostridium difficile from healthy food animals: optimized isolation and prevalence. Journal of Food Protection 74: 130133.
Tvede, M, Schiotz, PO and Krasilnikoff, PA (1990). Incidence of Clostridium difficile in hospitalized children. A prospective study. Acta Paediatrica Scandinavica 79: 292299.
United-Nations (2007). World ageing population: 1950–2050. Department of Economic and Social Affairs - Population Division. [Available online at http://www.un.org/esa/population/publications/worldageing19502050/] Last accessed November 19.
USDA United States Department of Agriculture – Food Safety and Inspection Service.Food Safety Education – Is it done yet? (2011) [Available online at: http://www.fsis.usda.gov/is_it_done_yet/brochure_text/index.asp#SMIT]. Last accessed November 19, 2012.
Uzal, FA, Diab, SS, Blanchard, P, Moore, J, Anthenill, L, Shahriar, F, Garcia, JP and Songer, JG (2011). Clostridium perfringens type C and Clostridium difficile co-infection in foals. Veterinary Microbiology 156: 395402.
Warny, M, Pepin, J, Fang, A, Killgore, G, Thompson, A, Brazier, J, Frost, E and McDonald, LC (2005). Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe. Lancet 366: 10791084.
Weese, JS (2010). Clostridium difficile in food – innocent bystander or serious threat? Clinical Microbiology and Infection 16: 310.
Weese, JS and Armstrong, J (2003). Outbreak of Clostridium difficile-associated disease in a small animal veterinary teaching hospital. Journal of Veterinary Internal Medicine 17: 813816.
Weese, JS, Avery, BP, Rousseau, J and Reid-Smith, R (2009). Detection and enumeration of Clostridium difficile spores in retail beef and pork. Applied and Environmental Microbiology 75: 50095011.
Weese, JS, Finley, R, Reid-Smith, RR, Janecko, Nand Rousseau, J (2010a). Evaluation of Clostridium difficile in dogs and the household environment. Epidemiology and Infection 105: 11001104.
Weese, JS, Reid-Smith, RJ, Avery, BP and Rousseau, J (2010b). Detection and characterization of Clostridium difficile in retail chicken. Letters in Applied Microbiology 50: 362365.
Weese, JS, Rousseau, J and Arroyo, L (2005). Bacteriological evaluation of commercial canine and feline raw diets. Canadian Veterinary Journal 46: 513516.
Weese, JS, Rousseau, J, Deckert, A, Gow, S and Reid-Smith, RJ (2011). Clostridium difficile and methicillin-resistant Staphylococcus aureus shedding by slaughter-age pigs. BMC Veterinary Research 7: 41.
Weese, JS, Toxopeus, L and Arroyo, L (2006). Clostridium difficile associated diarrhoea in horses within the community: predictors, clinical presentation and outcome. Equine Veterinary Journal 38: 185188.
Weese, JS, Weese, HE, Bourdeau, TL and Staempfli, HR (2001). Suspected Clostridium difficile-associated diarrhea in two cats. Journal of the American Veterinary Medical Association 218: 14361439, 1421.
Wilcox, MH (2004). Descriptive study of intravenous immunoglobulin for the treatment of recurrent Clostridium difficile diarrhoea. Journal of Antimicrobial Chemotherapy 53: 882884.
Wilcox, MH, Cunniffe, JG, Trundle, C and Redpath, C (1996). Financial burden of hospital-acquired Clostridium difficile infection. Journal of Hospital Infection 34: 2330.
Wilcox, MH, Fawley, WN, Settle, CD and Davidson, A (1998). Recurrence of symptoms in Clostridium difficile infection–relapse or reinfection? Journal of Hospital Infection 38: 93100.
Wysowski, DK (2007). Surveillance of prescription drug-related mortality using death certificate data. Drug Safety 30: 533540.
Zidaric, V, Pardon, B, Dos Vultos, T, Deprez, P, Brouwer, MS, Roberts, AP, Henriques, AO and Rupnik, M (2012). Different antibiotic resistance and sporulation properties within multiclonal Clostridium difficile PCR ribotypes 078, 126, and 033 in a single calf farm. Applied and Environmental Microbiology 78: 85158522.
Zidaric, V, MZemljic, M, Janezic, S, Kocuvan, A and Rupnik, M (2008). High diversity of Clostridium difficile genotypes isolated from a single poultry farm producing replacement laying hens. Anaerobe 14: 325327.
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Animal Health Research Reviews
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