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Published in: BMC Public Health 1/2014

Open Access 01-12-2014 | Research article

Prevalence of Clostridium difficilein raw beef, cow, sheep, goat, camel and buffalo meat in Iran

Authors: Ebrahim Rahimi, Mohammad Jalali, J Scott Weese

Published in: BMC Public Health | Issue 1/2014

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Abstract

Background

Clostridium difficile has been shown to be a nosocomial pathogen associated with diarrhoea and pseudomembranous colitis in hospitalised patients and the infection is believed to be acquired nosocomially. Recent studies have shown the occurrence of C. difficile in food animals which may act as a source of infection to humans.The aim of this study was to determine the occurrence of C. difficile in retail raw beef, cow, sheep, goat, camel and buffalo meat in Iran.

Method

From April to October 2012, a total of 660 raw meat samples from beef, cow, sheep, goat, camel and buffalo were purchased from 49 butcheries in Isfahan and Khuzestan provinces, Iran, and were evaluated for the presence of C. difficile using a method including selective enrichment in C. difficile broth, subsequent alcohol shock-treatment and plating onto C. difficile selective medium. C. difficile isolates were tested for the presence of toxin genes and were typed using PCR ribotyping.

Results

In this study, 13 of 660 meat samples (2%) were contaminated with C. difficile. The highest prevalence of C. difficile was found in buffalo meat (9%), followed by goat meat (3.3%), beef meat (1.7%), cow (0.94%) and sheep meat (0.9%). Seven of the 13C. difficile strains (53.9%) were positive for tcdA, tcdB and cdtB toxin genes and were classified as ribotype 078. Four strains (30.8%) were positive tcdA, and tcdB, and one strain (7.7%) was possessed only tcdB. The remaining isolate was non-toxigenic. Susceptibilities of 13C. difficile isolates were determined for 11 antimicrobial drugs using the disk diffusion assay. Resistance to clindamycin, gentamycin, and nalidixic acid was the most common finding.

Conclusions

To our knowledge, the present study is the first report of the isolation of C. difficile from raw buffalo meat. This study indicates the potential importance of food, including buffalo meat, as a source of transmission of C. difficile to humans.
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Literature
1.
go back to reference Weese JS: Clostridium difficile in food-innocent bystander or serious threat?. Clin Microbiol Infect. 2010, 16: 3-10.CrossRefPubMed Weese JS: Clostridium difficile in food-innocent bystander or serious threat?. Clin Microbiol Infect. 2010, 16: 3-10.CrossRefPubMed
2.
go back to reference Bauer MP, Veenendaal D, Verhoef L, Bloembergen P, van Dissel JT, Kuijper EJ: Clinical and microbiological characteristics of community-onset Clostridium difficile infection in The Netherlands. Clin Microbiol Infect. 2009, 15: 1087-1092. 10.1111/j.1469-0691.2009.02853.x.CrossRefPubMed Bauer MP, Veenendaal D, Verhoef L, Bloembergen P, van Dissel JT, Kuijper EJ: Clinical and microbiological characteristics of community-onset Clostridium difficile infection in The Netherlands. Clin Microbiol Infect. 2009, 15: 1087-1092. 10.1111/j.1469-0691.2009.02853.x.CrossRefPubMed
3.
go back to reference Wilcox MH, Mooney L, Bendall R, Settle CD, Fawley WN: A case–control study of community-associated Clostridium difficile infection. J Antimicrob Chemother. 2008, 62: 388-396. 10.1093/jac/dkn163.CrossRefPubMed Wilcox MH, Mooney L, Bendall R, Settle CD, Fawley WN: A case–control study of community-associated Clostridium difficile infection. J Antimicrob Chemother. 2008, 62: 388-396. 10.1093/jac/dkn163.CrossRefPubMed
4.
go back to reference Harvey RB, Norman KN, Andrews K, Hume ME, Scanlan CM, Callaway TR, Anderson RC, Nisbet DJ: Clostridium difficile in poultry and poultry meat. Foodborne Pathog Dis. 2011, 8: 1321-1323. 10.1089/fpd.2011.0936.CrossRefPubMed Harvey RB, Norman KN, Andrews K, Hume ME, Scanlan CM, Callaway TR, Anderson RC, Nisbet DJ: Clostridium difficile in poultry and poultry meat. Foodborne Pathog Dis. 2011, 8: 1321-1323. 10.1089/fpd.2011.0936.CrossRefPubMed
5.
go back to reference Keessen EC, Gaastra W, Lipman LJA: Clostridium difficile infection in humans and animals, differences and similarities. Vet Microbiol. 2011, 153: 205-217. 10.1016/j.vetmic.2011.03.020.CrossRefPubMed Keessen EC, Gaastra W, Lipman LJA: Clostridium difficile infection in humans and animals, differences and similarities. Vet Microbiol. 2011, 153: 205-217. 10.1016/j.vetmic.2011.03.020.CrossRefPubMed
6.
go back to reference Simango C, Mwakurudza S: Clostridium difficile in broiler chickens sold at market places in Zimbabwe and their antimicrobial susceptibility. Int J Food Microbiol. 2008, 124: 268-270. 10.1016/j.ijfoodmicro.2008.03.020.CrossRefPubMed Simango C, Mwakurudza S: Clostridium difficile in broiler chickens sold at market places in Zimbabwe and their antimicrobial susceptibility. Int J Food Microbiol. 2008, 124: 268-270. 10.1016/j.ijfoodmicro.2008.03.020.CrossRefPubMed
7.
go back to reference Al Saif N, Brazier JS: The distribution of Clostridium difficile in the environment of South Wales. J Med Microbiol. 1996, 45: 133-137. 10.1099/00222615-45-2-133.CrossRefPubMed Al Saif N, Brazier JS: The distribution of Clostridium difficile in the environment of South Wales. J Med Microbiol. 1996, 45: 133-137. 10.1099/00222615-45-2-133.CrossRefPubMed
8.
go back to reference Songer JG, Trinh HT, Killgore GE, Thompson AD, McDonald LC, Limbago BM: Clostridium difficile in retail meat products, USA 2007. Emerg Infect Dis. 2009, 15: 819-821. 10.3201/eid1505.081071.CrossRefPubMedPubMedCentral Songer JG, Trinh HT, Killgore GE, Thompson AD, McDonald LC, Limbago BM: Clostridium difficile in retail meat products, USA 2007. Emerg Infect Dis. 2009, 15: 819-821. 10.3201/eid1505.081071.CrossRefPubMedPubMedCentral
9.
go back to reference Songer JG: Clostridia as agents of zoonotic disease. Vet Microbiol. 2010, 140: 399-404. 10.1016/j.vetmic.2009.07.003.CrossRefPubMed Songer JG: Clostridia as agents of zoonotic disease. Vet Microbiol. 2010, 140: 399-404. 10.1016/j.vetmic.2009.07.003.CrossRefPubMed
10.
go back to reference Rodriguez-Palacios A, Stämpfli HR, Duffield T, Peregrine AS, Trotz-Williams LA, Arroyo LG, Brazier JS, Weese JS: Clostridium difficile PCR ribotypes in calves, Canada. Emerg Infect Dis. 2006, 12: 1730-1736. 10.3201/eid1211.051581.CrossRefPubMedPubMedCentral Rodriguez-Palacios A, Stämpfli HR, Duffield T, Peregrine AS, Trotz-Williams LA, Arroyo LG, Brazier JS, Weese JS: Clostridium difficile PCR ribotypes in calves, Canada. Emerg Infect Dis. 2006, 12: 1730-1736. 10.3201/eid1211.051581.CrossRefPubMedPubMedCentral
11.
go back to reference Goorhuis A, Debast SB, Van Leengoed LA, Harmanus C, Notermans DW, Bergwerff AA, Kuijper EJ: Clostridium difficile PCR ribotype 078: an emerging strain in humans and in pigs?. J ClinMicrobiol. 2008, 46: 1157-1158. Goorhuis A, Debast SB, Van Leengoed LA, Harmanus C, Notermans DW, Bergwerff AA, Kuijper EJ: Clostridium difficile PCR ribotype 078: an emerging strain in humans and in pigs?. J ClinMicrobiol. 2008, 46: 1157-1158.
12.
go back to reference Rupnik M, Wilcox MH, Gerding DN: Clostridium difficile infection: new developments in epidemiology and pathogenesis. Natur Rev Microbiol. 2009, 7: 526-536. 10.1038/nrmicro2164.CrossRef Rupnik M, Wilcox MH, Gerding DN: Clostridium difficile infection: new developments in epidemiology and pathogenesis. Natur Rev Microbiol. 2009, 7: 526-536. 10.1038/nrmicro2164.CrossRef
13.
go back to reference Pirs T, Ocepek M, Rupnik M: Isolation of Clostridium difficile from food animals in Slovenia. J Med Microbiol. 2008, 57: 790-792. 10.1099/jmm.0.47669-0.CrossRefPubMed Pirs T, Ocepek M, Rupnik M: Isolation of Clostridium difficile from food animals in Slovenia. J Med Microbiol. 2008, 57: 790-792. 10.1099/jmm.0.47669-0.CrossRefPubMed
14.
go back to reference Jalali M, Khorvash F, Warriner K, Weese JS: Clostridium difficile infection in an Iranian hospital. BMC Res Notes. 2012, 5: 159-10.1186/1756-0500-5-159. 10.1186/1756-0500-5-159CrossRefPubMedPubMedCentral Jalali M, Khorvash F, Warriner K, Weese JS: Clostridium difficile infection in an Iranian hospital. BMC Res Notes. 2012, 5: 159-10.1186/1756-0500-5-159. 10.1186/1756-0500-5-159CrossRefPubMedPubMedCentral
15.
go back to reference Rodriguez-Palacios A, Staempfli HR, Duffield T, Weese JS: Clostridium difficile in retail ground meat Canada. Emerg Infect Dis. 2007, 13: 485-487. 10.3201/eid1303.060988.CrossRefPubMedPubMedCentral Rodriguez-Palacios A, Staempfli HR, Duffield T, Weese JS: Clostridium difficile in retail ground meat Canada. Emerg Infect Dis. 2007, 13: 485-487. 10.3201/eid1303.060988.CrossRefPubMedPubMedCentral
16.
go back to reference de Boer E, Zwartkruis-Nahuis A, Heuvelink AE, Harmanus C, Kuijper EJ: Prevalence of Clostridium difficile in retailed meat in The Netherlands. Int J Food Microbiol. 2011, 144: 561-564. 10.1016/j.ijfoodmicro.2010.11.007.CrossRefPubMed de Boer E, Zwartkruis-Nahuis A, Heuvelink AE, Harmanus C, Kuijper EJ: Prevalence of Clostridium difficile in retailed meat in The Netherlands. Int J Food Microbiol. 2011, 144: 561-564. 10.1016/j.ijfoodmicro.2010.11.007.CrossRefPubMed
17.
go back to reference Bidet P, Barbut F, Lalande V, Burghoffer B, Petit J: Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing. FEMS Microbiol Lett. 1999, 175: 261-266. 10.1111/j.1574-6968.1999.tb13629.x.CrossRefPubMed Bidet P, Barbut F, Lalande V, Burghoffer B, Petit J: Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing. FEMS Microbiol Lett. 1999, 175: 261-266. 10.1111/j.1574-6968.1999.tb13629.x.CrossRefPubMed
18.
go back to reference Lemee L, Dhalluin A, Testelin S, Mattrat M, Maillard K, Lemeland J, Pons JL: Multiplex PCR targeting tpi (triose phosphate isomerase), tcdA (Toxin A), and tcdB (Toxin B) genes for toxigenic culture of Clostridium difficile. J Clin Microbiol. 2004, 42: 5710-5714. 10.1128/JCM.42.12.5710-5714.2004.CrossRefPubMedPubMedCentral Lemee L, Dhalluin A, Testelin S, Mattrat M, Maillard K, Lemeland J, Pons JL: Multiplex PCR targeting tpi (triose phosphate isomerase), tcdA (Toxin A), and tcdB (Toxin B) genes for toxigenic culture of Clostridium difficile. J Clin Microbiol. 2004, 42: 5710-5714. 10.1128/JCM.42.12.5710-5714.2004.CrossRefPubMedPubMedCentral
19.
go back to reference Clinical and Laboratory Standards Institute (CLSI): Performance Standards for Antimicrobial Susceptibility Testing; 7th ed, CLSI document M11–A7. 2007, Wayne, PA: Clinical and Laboratory Standards Institute Clinical and Laboratory Standards Institute (CLSI): Performance Standards for Antimicrobial Susceptibility Testing; 7th ed, CLSI document M11–A7. 2007, Wayne, PA: Clinical and Laboratory Standards Institute
20.
go back to reference Rodriguez-Palacios A, Reid-Smith RJ, Staempfli HR, Daignault D, Janecko N, Avery BP, Martin H, Thompson AD, McDonald LC, Limbago B, Weese JS: Possibility of seasonality of Clostridium difficile in retail meat, Canada. Emerg Infect Dis. 2009, 15: 802-805. 10.3201/eid1505.081084.CrossRefPubMedPubMedCentral Rodriguez-Palacios A, Reid-Smith RJ, Staempfli HR, Daignault D, Janecko N, Avery BP, Martin H, Thompson AD, McDonald LC, Limbago B, Weese JS: Possibility of seasonality of Clostridium difficile in retail meat, Canada. Emerg Infect Dis. 2009, 15: 802-805. 10.3201/eid1505.081084.CrossRefPubMedPubMedCentral
21.
go back to reference Bouttier S, Barc MC, Felix B, Lambert S, Collignon A, Barbut F: Clostridium difficile in ground meat, France. Emerg Infect Dis. 2010, 16: 733-735. 10.3201/eid1604.091138.CrossRefPubMedPubMedCentral Bouttier S, Barc MC, Felix B, Lambert S, Collignon A, Barbut F: Clostridium difficile in ground meat, France. Emerg Infect Dis. 2010, 16: 733-735. 10.3201/eid1604.091138.CrossRefPubMedPubMedCentral
22.
go back to reference Jöbstl M, Heuberger S, Indra A, Nepf R, Köfer J, Wagner M: Clostridium difficile in raw products of animal origin. Int J Food Microbiol. 2010, 138: 172-175. 10.1016/j.ijfoodmicro.2009.12.022.CrossRefPubMed Jöbstl M, Heuberger S, Indra A, Nepf R, Köfer J, Wagner M: Clostridium difficile in raw products of animal origin. Int J Food Microbiol. 2010, 138: 172-175. 10.1016/j.ijfoodmicro.2009.12.022.CrossRefPubMed
23.
go back to reference Curry SR, Marsh JW, Schlackman JL, Harrison LH: Prevalence of Clostridium difficilein uncooked ground meat products from Pittsburgh, Pennsylvania. Appl Environ Microbiol. 2012, 78: 4183-4186. 10.1128/AEM.00842-12.CrossRefPubMedPubMedCentral Curry SR, Marsh JW, Schlackman JL, Harrison LH: Prevalence of Clostridium difficilein uncooked ground meat products from Pittsburgh, Pennsylvania. Appl Environ Microbiol. 2012, 78: 4183-4186. 10.1128/AEM.00842-12.CrossRefPubMedPubMedCentral
24.
go back to reference Von Abercron SMM, Karlsson F, Wigh GT, Wierup M, Krovacek K: Low occurrence of Clostridium difficile in retail ground meat in Sweden. J Food Prot. 2009, 72: 1732-1734.PubMed Von Abercron SMM, Karlsson F, Wigh GT, Wierup M, Krovacek K: Low occurrence of Clostridium difficile in retail ground meat in Sweden. J Food Prot. 2009, 72: 1732-1734.PubMed
25.
go back to reference Baker AA, Davis E, Rehberger T, Rosener D: Prevalence and diversity of toxigenic Clostridium perfringens and Clostridium difficile among swine herds in the midwest. Appl Environ Microbiol. 2010, 76: 2961-2967. 10.1128/AEM.02459-09.CrossRefPubMedPubMedCentral Baker AA, Davis E, Rehberger T, Rosener D: Prevalence and diversity of toxigenic Clostridium perfringens and Clostridium difficile among swine herds in the midwest. Appl Environ Microbiol. 2010, 76: 2961-2967. 10.1128/AEM.02459-09.CrossRefPubMedPubMedCentral
26.
go back to reference Thitaram SN, Frank JF, Lyon SA, Siragusa GR, Bailey JS, Lombard JE, Haley CA, Wagner BA, Dargatz DA, Fedorka-Cray PJ: Clostridium difficile from healthy food animals: optimized isolation and prevalence. J Food Prot. 2011, 74: 130-133. 10.4315/0362-028X.JFP-10-229.CrossRefPubMed Thitaram SN, Frank JF, Lyon SA, Siragusa GR, Bailey JS, Lombard JE, Haley CA, Wagner BA, Dargatz DA, Fedorka-Cray PJ: Clostridium difficile from healthy food animals: optimized isolation and prevalence. J Food Prot. 2011, 74: 130-133. 10.4315/0362-028X.JFP-10-229.CrossRefPubMed
27.
go back to reference Avbersek J, Janezic S, Pate M, Rupnik M, Zidaric V, Logar K, Vengust M, Zemljic M, Pirs T, Ocepek M: Diversity of Clostridium difficile in pigs and other animals in Slovenia. Anaerobe. 2009, 15: 252-255. 10.1016/j.anaerobe.2009.07.004.CrossRefPubMed Avbersek J, Janezic S, Pate M, Rupnik M, Zidaric V, Logar K, Vengust M, Zemljic M, Pirs T, Ocepek M: Diversity of Clostridium difficile in pigs and other animals in Slovenia. Anaerobe. 2009, 15: 252-255. 10.1016/j.anaerobe.2009.07.004.CrossRefPubMed
28.
go back to reference Indra A, Schmid D, Huhulescu S, Hell M, Gattringer R, Hasenberger P, Fiedler A, Wewalka G, Allerberger F: Characterization of clinical Clostridium difficile isolates by PCR ribotyping and detection of toxin genes in Austria, 2006–2007. J Med Microbiol. 2008, 57: 702-708. 10.1099/jmm.0.47476-0.CrossRefPubMed Indra A, Schmid D, Huhulescu S, Hell M, Gattringer R, Hasenberger P, Fiedler A, Wewalka G, Allerberger F: Characterization of clinical Clostridium difficile isolates by PCR ribotyping and detection of toxin genes in Austria, 2006–2007. J Med Microbiol. 2008, 57: 702-708. 10.1099/jmm.0.47476-0.CrossRefPubMed
29.
go back to reference Rahimi E, Momtaz H, Bonyadian M: PCR detection of Campylobacter sp. from turkey carcasses during processing plant in Iran. Food Control. 2010, 21: 692-694. 10.1016/j.foodcont.2009.10.009.CrossRef Rahimi E, Momtaz H, Bonyadian M: PCR detection of Campylobacter sp. from turkey carcasses during processing plant in Iran. Food Control. 2010, 21: 692-694. 10.1016/j.foodcont.2009.10.009.CrossRef
30.
go back to reference Rahimi E, Momtaz H, Ameri M, Ghasemian Safai H, Ali Kazemi M: Prevalence and antimicrobial resistance of Campylobacter species isolated from chicken carcasses during processing in Iran. Poult Sci. 2010, 89: 1015-1020. 10.3382/ps.2009-00090.CrossRefPubMed Rahimi E, Momtaz H, Ameri M, Ghasemian Safai H, Ali Kazemi M: Prevalence and antimicrobial resistance of Campylobacter species isolated from chicken carcasses during processing in Iran. Poult Sci. 2010, 89: 1015-1020. 10.3382/ps.2009-00090.CrossRefPubMed
31.
go back to reference Rahimi E, Momtaz H, Nozarpour N: Prevalence of Listeria spp., Campylobacter spp., and Escherichia coli O157:H7 isolated from camel during processing. BJVM. 2010, 13: 179-185. Rahimi E, Momtaz H, Nozarpour N: Prevalence of Listeria spp., Campylobacter spp., and Escherichia coli O157:H7 isolated from camel during processing. BJVM. 2010, 13: 179-185.
Metadata
Title
Prevalence of Clostridium difficilein raw beef, cow, sheep, goat, camel and buffalo meat in Iran
Authors
Ebrahim Rahimi
Mohammad Jalali
J Scott Weese
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Public Health / Issue 1/2014
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/1471-2458-14-119

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