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Clostridium difficile: Is it a New Food-Borne Pathogen?

Year 2018, Volume: 13 Issue: 3, 389 - 396, 25.12.2018
https://doi.org/10.17094/ataunivbd.364311

Abstract

Clostridium difficile, commonly found in nature, is a nosocomial opportunistic pathogen which causes formation of various clinical disorders including antibiotic associated diarrhea, fulminant colitis and pseudomembranous colitis. C. difficile is thought to be responsible for almost all of the pseudomembranous colitis and 15-25% of the antibiotics related diarrhea. Also it is known that hypervirulent strains generally have high recurrence rate and cause severe infections or even death. Although there is not enough data that C.difficile infects people by transmition via food, there is a significant increase in infections caused by C. difficile in recent studies. In addition to this knowledge bacteria have been isolated from various samples which animal foods, raw or ready to eat foods, vegetables, salads, the waters of sea, lake and river, seafood, soil and environmental samples. All of these bring to mind a question that C. difficile is whether or not a food-borne pathogen. Toxigenic characteristics of some strains of C. difficile detected in foods, resistance to antibiotics in various ratios and their spreading easily properties due to endospores resistant to difficult conditions have further increased the importance of this bacterium. In this review, the information about general characteristics, pathogenesis, infection sources, risk factors, presence in food, isolation from food and idendification of C. difficile have been given.

References

  • 1. Cartman ST., Heap JT., Kuehne SA., Cockayne A., Minton NP., 2010. The emergence of ‘hypervirulence’ in Clostridium difficile. Int. J. Med. Microbiol., 300, 387-395.
  • 2. Barbut F., Petit JC., 2001. Epidemiology of Clostridium difficile-associated infections. Clinic. Microbiol. Infect., 7(8), 405-410.
  • 3. Weese JS., 2010. Clostridium difficile in food—innocent bystander or serious threat? Clin. Microbiol. Infect., 16, 3–10.
  • 4. Kıyan M., 1999. Anaerop, sporlu, gram pozitif basiller. In “Temel ve Klinik Mikrobiyoloji”, Ed., Ustaçelebi Ş., Ankara, Güneş Kitabevi, 645-649.
  • 5. Kelly CP., LaMont JT., 2008. Clostridium difficile — More difficult than ever. N. Engl. J. Med., 359, 1932-1940.
  • 6. Karadağ FY., 2013. Clostridium difficile. Ekmud Bilimsel Platformu. 20-24 Mart 2013, Antalya, 32-33.
  • 7. Rainey FA., Hollen BJ., Small A., 2009. Clostridium, In “Bergey’s Manual of Systematic Bacteriology”, Ed., Vos PD., Garrity GM., Jones D., Krieg NR., Ludwig W., Rainey FA., Schleifer KH., Whitman WB., 2th ed, volume III. USA, 736-828.
  • 8. Vedantam G., Clark A., Chu M., McQuade R., Mallozzi M., Viswanathan VK., 2012. Clostridium difficile infection: Toxins and non-toxin virulence factors, and their contributions to disease establishment and host response. Gut Microbes, March/April, 121–134.
  • 9. 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., Eichel-Streiber C., 2005. Revised nomenclature of Clostridium difficile toxins and associated genes. J. Med. Microbiol., 54, 113–117.
  • 10. Lawley TD., Croucher NJ., Yu L., Clare S., Sebaihia M., Goulding D., Pickard DJ., Parkhill J., Choudhary J., Dougan G., 2009. Proteomic and genomic characterization of highly infectious Clostridium difficile 630 spores. J. Bacteriol., 191, 5377-5386.
  • 11. Cookson B., 2007. Hypervirulent strains of Clostridium difficile. Postgrad. Med. J., 83, 291-295.
  • 12. Sinh P., Barrett TA., Yun L., 2011. Clostridium difficile infection and inflammatory bowel disease: a review. Gastroenterol. Res. Pract., 11.
  • 13. Kılıç A., 2013. Clostridium difficile Enfeksiyonu: Epidemiyoloji, risk faktörleri, patogenez, klinik özellikler, tanı ve tedavi. Mikrobiyol Bul., 47(3), 556-566.
  • 14. Peláez T., Alcalá L., Alonso R., Rodríguez-Créixems M., García-Lechuz JM., Bouza E., 2002. Susceptibility to metronidazole and reassessment of Clostridium difficile vancomycin. Antimicrob. Agents. Ch., 46(6), 1647–1650.
  • 15. Dworczyński A., Sokoł B., Meisel-Mikołajczyk F., 1991. Antibiotic resistance of Clostridium difficile isolates. Cytobios., 65, 149-153.
  • 16. Jöbstl M., Heuberger S., Indra A., Nepf R., Köfer J., Wagner M., 2010. Clostridium difficile in raw products of animal origin. Int. J. Food Microbiol., 138, 172–175.
  • 17. Metcalf DS., Costa MC., Dew WMV., Weese JS., 2010. Clostridium difficile in vegetables, Canada. Lett. Appl. Microbiol., 51, 600–602.
  • 18. Bakri MM., Brown DJ., Butcher JP., Sutherland AD., 2009. Clostridium difficile in ready-to-eat salads, Scotland. Emerg. Infect. Dis., 15(5), 817-818.
  • 19. Simango C., Mwakurudza S., 2008. Clostridium difficile in broiler chickens sold at market places in Zimbabwe and their antimicrobial susceptibility. Int. J. Food. Microbiol., 124, 268–270.
  • 20. Planche T., Arnold A., 2009. Clostridium difficile. Medicine, 37(12), 641-643.
  • 21. Wilson BA., Salyers AA., Whitt DD., Winkler ME., 2011. Bacterial Pathogenesis: A Molecular Approach. 3th ed, Washington, ASM Press, 423-431.
  • 22. McFee RB., Abdelsayed GG., 2009. Clostridium difficile. Dis. Mon., 55, 439-470.
  • 23. Rupnik M., 2010. Clostridium difficile: (Re)emergence of zoonotic potential. Clin. Infect. Dis., 51(5), 583–584.
  • 24. Leffler DA., Lamont JT., 2015. Clostridium difficile Infection. N Engl J Med. 372,1539-48.
  • 25. Leclair MA., Allard C., Lesur O., Pépin J., 2010. Clostridium difficile infection in the intensive care unit. J. Intensive Care Med., 25(1), 23-30.
  • 26. Gordon D., Young LR., Reddy S., Bergman C., Young JD., 2016. Incidence of Clostridium difficile infection in patients receiving high-risk antibiotics with or without a proton pump inhibitor. J. Hosp. Infect., 92, 173-177.
  • 27. Broda DM., DeLacy KM., Bell RG., Braggins TJ., 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. Int. J. of Food Microbiol., 29, 335–352.
  • 28. Eckert C., Burghoffer B., Barbut F., 2013. Contamination of ready-to-eat raw vegetables with Clostridium difficile in France. J. Med. Microbiol., 62, 1435–1438.
  • 29. Rodriguez C., Korsak N., Taminiau B., Avesani V., Van Broeck J., Brach P., Delmee M., Daube G., 2015. Clostridium difficile from food and surface samples in a Belgian nursing home: An unlikely source of contamination. Anaerobe, 32, 87-89.
  • 30. Rahimi E., Afzali ZS., Baghbadorani ZT., 2015. Clostridium difficile in ready-to-eat foods in Isfahan and Shahrekord, Iran. Asian Pac. J. Trop. Biomed., 5(2), 128-131.
  • 31. Esfandiari Z., Weese S., Ezzatpanah H., Jalali M., Chamani M., 2014. Occurrence of Clostridium difficile in seasoned hamburgers and seven processing plants in Iran. BMC Microbiology., 14, 283.
  • 32. Metcalf D., Avery BP., Janecko N., Matic N., Reid-Smith R., Weese JS., 2011. Clostridium difficile in seafood and fish. Anaerobe, 17, 85-86.
  • 33. Montazeri N., Liu D., Janes ME., 2015. Occurrence of toxigenic Clostridium difficile in Louisiana Oysters (Crassostrea virginica) and environmental waters. Food Nutr. Sci., 6, 1065-1070.
  • 34. Rodriguez-Palacios A., Staempfli HR., Duffield T., Weese JS., 2007. Clostridium difficile in retail ground meat, Canada. Emerg. Infect. Dis., 13(3), 485-487.
  • 35. Weese JS., Reid-Smith RJ., Avery BP., Rousseau J., 2010. Detection and characterization of Clostridium difficile in retail chicken Lett. Appl. Microbiol., 50, 362–365.
  • 36. Drigo I., Mazzolini E., Bacchin C., Tonon E., Puiatti C., Bano L., Spigaglia P., Barbanti F., Agnoletti F., 2015. Molecular characterization and antimicrobial susceptibility of Clostridium difficile isolated from rabbits raised for meat production. Vet. Microbiol., 181, 303–307.
  • 37. Boer E., Zwartkruis-Nahuis A., Heuvelink AE., Harmanus C., Kuijper EJ., 2011. Prevalence of Clostridium difficile in retailed meat in the Netherlands. Int. J. Food Microbiol., 144(3), 561–564.
  • 38. Güran HS., İlhak OI., 2015. Clostridium difficile in retail chicken meat parts and liver in the Eastern Region of Turkey. J. Verbr. Lebensm., 10, 359–364.
  • 39. Rahimi E., Jalali M., Weese JS., 2014. Prevalence of Clostridium difficile in raw beef,cow, sheep, goat, camel and buffalo meat in Iran. BMC Public Health, 14, 119.
  • 40. Songer JG., Trinh HT., Killgore GE., Thompson AD., McDonald LC., Limbago BM., 2009. Clostridium difficile in retail meat products, USA, 2007. Emerg. Infect. Dis,. 2009, 15(5), 819-821.
  • 41. Brazier JS., 1998. The diagnosis of Clostridium difficile-associated disease. J. Antimicrob. Chemother., 41, Suppl. C, 29–40.
  • 42. Selmer T., Andrei PI., 2001. p-Hydroxyphenylacetate decarboxylase from Clostridium difficile. A novel glycyl radical enzyme catalysing the formation of p-cresol. Eur. J. Biochem., 268, 1363-1372.
  • 43. Yıldız F., Gücükoğlu A., 2012. Clostridium difficile ve gıda güvenliği açısından önemi. Elektronik Mikrobiyoloji Derg., 10(1), 22-29.
  • 44. Fedorko DP., Williams EC., 1997. Use of cycloserine-cefoxitin-fructose Agar and L-Proline–Aminopeptidase (PRO Discs) in the rapid identification of Clostridium difficile. J. of Clin. Microbiol., 35(5), 1258–1259.

Clostridium difficile: Yeni Bir Gıda Patojeni mi?

Year 2018, Volume: 13 Issue: 3, 389 - 396, 25.12.2018
https://doi.org/10.17094/ataunivbd.364311

Abstract

Doğada yaygın olarak bulunan Clostridium difficile, antibiyotik ilişkili ishal, pseudomembranöz kolit ve fulminant kolit olmak üzere çeşitli klinik tabloların şekillenmesine sebep olabilen nozokomiyal fırsatçı bir patojendir. Antibiyotiğe bağlı ishallerin %15-25’inden, psödomembranöz kolitlerin hemen hemen hepsinden sorumlu olduğu düşünülen C. difficile’in hipervirülan suşlarının ise genellikle nüks oranı yüksek ve şiddetli enfeksiyonlara hatta ölüme yol açtıkları bilinmektedir. C. difficile’in gıdalardan insanlara bulaşarak enfeksiyon yaptığına dair henüz yeterli veri bulunmamakla birlikte son yıllarda yapılan çalışmalarda C. difficile enfeksiyonlarında çarpıcı bir artış olduğunun belirtilmesi, etkenin aynı zamanda hayvansal gıdalardan, çiğ veya tüketime hazır gıdalardan, sebzelerden, salatalardan, deniz, göl ve nehir sularından, su ürünlerinden, topraktan ve çeşitli çevresel numunelerden izole edilmiş olması, C. difficile’in gıda kaynaklı bir patojen olup olmadığı sorusunu akla getirmektedir. C. difficile’in gıdalarda tespit edilen bazı suşlarının toksijenik özellik taşımaları, antibiyotiklere karşı değişen oranlarda dirençli olmaları ve zor şartlara dayanıklı endosporları sayesinde kolayca yayılabilme özellikleri ise bu bakterinin önemini giderek arttırmaktadır. Bu derlemede C. difficile’in genel özellikleri, patojenitesi, enfeksiyon kaynakları, risk faktörleri, gıdalarda varlığı, gıdalardan izolasyonu ve identifikasyonu hakkında bilgilere yer verilmiştir. 

References

  • 1. Cartman ST., Heap JT., Kuehne SA., Cockayne A., Minton NP., 2010. The emergence of ‘hypervirulence’ in Clostridium difficile. Int. J. Med. Microbiol., 300, 387-395.
  • 2. Barbut F., Petit JC., 2001. Epidemiology of Clostridium difficile-associated infections. Clinic. Microbiol. Infect., 7(8), 405-410.
  • 3. Weese JS., 2010. Clostridium difficile in food—innocent bystander or serious threat? Clin. Microbiol. Infect., 16, 3–10.
  • 4. Kıyan M., 1999. Anaerop, sporlu, gram pozitif basiller. In “Temel ve Klinik Mikrobiyoloji”, Ed., Ustaçelebi Ş., Ankara, Güneş Kitabevi, 645-649.
  • 5. Kelly CP., LaMont JT., 2008. Clostridium difficile — More difficult than ever. N. Engl. J. Med., 359, 1932-1940.
  • 6. Karadağ FY., 2013. Clostridium difficile. Ekmud Bilimsel Platformu. 20-24 Mart 2013, Antalya, 32-33.
  • 7. Rainey FA., Hollen BJ., Small A., 2009. Clostridium, In “Bergey’s Manual of Systematic Bacteriology”, Ed., Vos PD., Garrity GM., Jones D., Krieg NR., Ludwig W., Rainey FA., Schleifer KH., Whitman WB., 2th ed, volume III. USA, 736-828.
  • 8. Vedantam G., Clark A., Chu M., McQuade R., Mallozzi M., Viswanathan VK., 2012. Clostridium difficile infection: Toxins and non-toxin virulence factors, and their contributions to disease establishment and host response. Gut Microbes, March/April, 121–134.
  • 9. 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., Eichel-Streiber C., 2005. Revised nomenclature of Clostridium difficile toxins and associated genes. J. Med. Microbiol., 54, 113–117.
  • 10. Lawley TD., Croucher NJ., Yu L., Clare S., Sebaihia M., Goulding D., Pickard DJ., Parkhill J., Choudhary J., Dougan G., 2009. Proteomic and genomic characterization of highly infectious Clostridium difficile 630 spores. J. Bacteriol., 191, 5377-5386.
  • 11. Cookson B., 2007. Hypervirulent strains of Clostridium difficile. Postgrad. Med. J., 83, 291-295.
  • 12. Sinh P., Barrett TA., Yun L., 2011. Clostridium difficile infection and inflammatory bowel disease: a review. Gastroenterol. Res. Pract., 11.
  • 13. Kılıç A., 2013. Clostridium difficile Enfeksiyonu: Epidemiyoloji, risk faktörleri, patogenez, klinik özellikler, tanı ve tedavi. Mikrobiyol Bul., 47(3), 556-566.
  • 14. Peláez T., Alcalá L., Alonso R., Rodríguez-Créixems M., García-Lechuz JM., Bouza E., 2002. Susceptibility to metronidazole and reassessment of Clostridium difficile vancomycin. Antimicrob. Agents. Ch., 46(6), 1647–1650.
  • 15. Dworczyński A., Sokoł B., Meisel-Mikołajczyk F., 1991. Antibiotic resistance of Clostridium difficile isolates. Cytobios., 65, 149-153.
  • 16. Jöbstl M., Heuberger S., Indra A., Nepf R., Köfer J., Wagner M., 2010. Clostridium difficile in raw products of animal origin. Int. J. Food Microbiol., 138, 172–175.
  • 17. Metcalf DS., Costa MC., Dew WMV., Weese JS., 2010. Clostridium difficile in vegetables, Canada. Lett. Appl. Microbiol., 51, 600–602.
  • 18. Bakri MM., Brown DJ., Butcher JP., Sutherland AD., 2009. Clostridium difficile in ready-to-eat salads, Scotland. Emerg. Infect. Dis., 15(5), 817-818.
  • 19. Simango C., Mwakurudza S., 2008. Clostridium difficile in broiler chickens sold at market places in Zimbabwe and their antimicrobial susceptibility. Int. J. Food. Microbiol., 124, 268–270.
  • 20. Planche T., Arnold A., 2009. Clostridium difficile. Medicine, 37(12), 641-643.
  • 21. Wilson BA., Salyers AA., Whitt DD., Winkler ME., 2011. Bacterial Pathogenesis: A Molecular Approach. 3th ed, Washington, ASM Press, 423-431.
  • 22. McFee RB., Abdelsayed GG., 2009. Clostridium difficile. Dis. Mon., 55, 439-470.
  • 23. Rupnik M., 2010. Clostridium difficile: (Re)emergence of zoonotic potential. Clin. Infect. Dis., 51(5), 583–584.
  • 24. Leffler DA., Lamont JT., 2015. Clostridium difficile Infection. N Engl J Med. 372,1539-48.
  • 25. Leclair MA., Allard C., Lesur O., Pépin J., 2010. Clostridium difficile infection in the intensive care unit. J. Intensive Care Med., 25(1), 23-30.
  • 26. Gordon D., Young LR., Reddy S., Bergman C., Young JD., 2016. Incidence of Clostridium difficile infection in patients receiving high-risk antibiotics with or without a proton pump inhibitor. J. Hosp. Infect., 92, 173-177.
  • 27. Broda DM., DeLacy KM., Bell RG., Braggins TJ., 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. Int. J. of Food Microbiol., 29, 335–352.
  • 28. Eckert C., Burghoffer B., Barbut F., 2013. Contamination of ready-to-eat raw vegetables with Clostridium difficile in France. J. Med. Microbiol., 62, 1435–1438.
  • 29. Rodriguez C., Korsak N., Taminiau B., Avesani V., Van Broeck J., Brach P., Delmee M., Daube G., 2015. Clostridium difficile from food and surface samples in a Belgian nursing home: An unlikely source of contamination. Anaerobe, 32, 87-89.
  • 30. Rahimi E., Afzali ZS., Baghbadorani ZT., 2015. Clostridium difficile in ready-to-eat foods in Isfahan and Shahrekord, Iran. Asian Pac. J. Trop. Biomed., 5(2), 128-131.
  • 31. Esfandiari Z., Weese S., Ezzatpanah H., Jalali M., Chamani M., 2014. Occurrence of Clostridium difficile in seasoned hamburgers and seven processing plants in Iran. BMC Microbiology., 14, 283.
  • 32. Metcalf D., Avery BP., Janecko N., Matic N., Reid-Smith R., Weese JS., 2011. Clostridium difficile in seafood and fish. Anaerobe, 17, 85-86.
  • 33. Montazeri N., Liu D., Janes ME., 2015. Occurrence of toxigenic Clostridium difficile in Louisiana Oysters (Crassostrea virginica) and environmental waters. Food Nutr. Sci., 6, 1065-1070.
  • 34. Rodriguez-Palacios A., Staempfli HR., Duffield T., Weese JS., 2007. Clostridium difficile in retail ground meat, Canada. Emerg. Infect. Dis., 13(3), 485-487.
  • 35. Weese JS., Reid-Smith RJ., Avery BP., Rousseau J., 2010. Detection and characterization of Clostridium difficile in retail chicken Lett. Appl. Microbiol., 50, 362–365.
  • 36. Drigo I., Mazzolini E., Bacchin C., Tonon E., Puiatti C., Bano L., Spigaglia P., Barbanti F., Agnoletti F., 2015. Molecular characterization and antimicrobial susceptibility of Clostridium difficile isolated from rabbits raised for meat production. Vet. Microbiol., 181, 303–307.
  • 37. Boer E., Zwartkruis-Nahuis A., Heuvelink AE., Harmanus C., Kuijper EJ., 2011. Prevalence of Clostridium difficile in retailed meat in the Netherlands. Int. J. Food Microbiol., 144(3), 561–564.
  • 38. Güran HS., İlhak OI., 2015. Clostridium difficile in retail chicken meat parts and liver in the Eastern Region of Turkey. J. Verbr. Lebensm., 10, 359–364.
  • 39. Rahimi E., Jalali M., Weese JS., 2014. Prevalence of Clostridium difficile in raw beef,cow, sheep, goat, camel and buffalo meat in Iran. BMC Public Health, 14, 119.
  • 40. Songer JG., Trinh HT., Killgore GE., Thompson AD., McDonald LC., Limbago BM., 2009. Clostridium difficile in retail meat products, USA, 2007. Emerg. Infect. Dis,. 2009, 15(5), 819-821.
  • 41. Brazier JS., 1998. The diagnosis of Clostridium difficile-associated disease. J. Antimicrob. Chemother., 41, Suppl. C, 29–40.
  • 42. Selmer T., Andrei PI., 2001. p-Hydroxyphenylacetate decarboxylase from Clostridium difficile. A novel glycyl radical enzyme catalysing the formation of p-cresol. Eur. J. Biochem., 268, 1363-1372.
  • 43. Yıldız F., Gücükoğlu A., 2012. Clostridium difficile ve gıda güvenliği açısından önemi. Elektronik Mikrobiyoloji Derg., 10(1), 22-29.
  • 44. Fedorko DP., Williams EC., 1997. Use of cycloserine-cefoxitin-fructose Agar and L-Proline–Aminopeptidase (PRO Discs) in the rapid identification of Clostridium difficile. J. of Clin. Microbiol., 35(5), 1258–1259.
There are 44 citations in total.

Details

Primary Language Turkish
Subjects Health Care Administration
Journal Section Derlemeler
Authors

Zeynep Alataş

Ahmet Güner

Publication Date December 25, 2018
Published in Issue Year 2018 Volume: 13 Issue: 3

Cite

APA Alataş, Z., & Güner, A. (2018). Clostridium difficile: Yeni Bir Gıda Patojeni mi?. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, 13(3), 389-396. https://doi.org/10.17094/ataunivbd.364311
AMA Alataş Z, Güner A. Clostridium difficile: Yeni Bir Gıda Patojeni mi?. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. December 2018;13(3):389-396. doi:10.17094/ataunivbd.364311
Chicago Alataş, Zeynep, and Ahmet Güner. “Clostridium Difficile: Yeni Bir Gıda Patojeni Mi?”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 13, no. 3 (December 2018): 389-96. https://doi.org/10.17094/ataunivbd.364311.
EndNote Alataş Z, Güner A (December 1, 2018) Clostridium difficile: Yeni Bir Gıda Patojeni mi?. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 13 3 389–396.
IEEE Z. Alataş and A. Güner, “Clostridium difficile: Yeni Bir Gıda Patojeni mi?”, Atatürk Üniversitesi Veteriner Bilimleri Dergisi, vol. 13, no. 3, pp. 389–396, 2018, doi: 10.17094/ataunivbd.364311.
ISNAD Alataş, Zeynep - Güner, Ahmet. “Clostridium Difficile: Yeni Bir Gıda Patojeni Mi?”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 13/3 (December 2018), 389-396. https://doi.org/10.17094/ataunivbd.364311.
JAMA Alataş Z, Güner A. Clostridium difficile: Yeni Bir Gıda Patojeni mi?. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2018;13:389–396.
MLA Alataş, Zeynep and Ahmet Güner. “Clostridium Difficile: Yeni Bir Gıda Patojeni Mi?”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, vol. 13, no. 3, 2018, pp. 389-96, doi:10.17094/ataunivbd.364311.
Vancouver Alataş Z, Güner A. Clostridium difficile: Yeni Bir Gıda Patojeni mi?. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2018;13(3):389-96.