Prevalence and Antibiotic Resistance of Clostridioides (Clostridium difficile) In Meat and Meat Products: A Systematic Review and Meta-Analysis
-
Zahra Esfandiari
,
Parisa Shoaei
,
Bahareh Vakili
,
Ziba Farajzadegan
,
Mohammad Javad Tarrahi
,
Zahra Emami
,
Yadolah Fakhri
,
J. Scott Weese
,
Trias Mahmudiono
Abstract
Background: Meat and meat products are introduced as one of the carriers of Clostridioides difficile. This study aimed to determine the prevalence and antibiotic resistance of C. difficile isolates in meat and meat products using a systematic review and meta-analysis.
Methods: It was performed a literature search in the primary international and bibliographic databases such as MEDLINE (PubMed), Cochrane Library, Embase, Scopus, and Web of Science to achieve all articles related to the prevalence and antibiotic resistance rates with no time restriction. A total of 54 studies examined C. difficile in 15,010 samples and its resistance to 10 antibiotics.
Results: The pooled prevalence of C. difficile was 3.4% in all samples. C. difficile pooled prevalence was detected in fish, poultry, and red meat samples with 6.9%, 5.2%, and 3.2%, respectively. Regarding antibiotic resistance, the highest pooled prevalence was for ciprofloxacin (86.6%), followed by clindamycin (42.6%) and erythromycin (34%). The lowest pooled prevalence was observed in metronidazole (7.6%), vancomycin (6.6%), and chloramphenicol (6%). We found low resistance to commonly used drugs for C. difficile infection treatment.
Conclusions: Every antibiotic can be a risk factor for CDI development, and drugs such as clindamycin, cephalosporins, and lately fluoroquinolones carry the highest risk. Therefore, we recommend the rational use of antibiotics in veterinary and human medicine
1. Lu Cl, Li HX, Zhu XY, et al (2022). Regula-tory effect of intracellular polysaccharides from Antrodia cinnamomea on the intes-tinal microbiota of mice with antibiotic-associated diarrhea. Qual Assur Saf Crops Foods, 14(3): 124-134.
2. Lawson PA, Citron DM, Tyrrell KL, et al (2016). Reclassification of Clostridium dif-ficile as Clostridioides difficile (Hall and O'Toole 1935) Prevot 1938. Anaerobe, 40: 95-9.
3. Weiss K (2009). Toxin binding treatment for clostridium difficile: a review including reports of studies with tolevamer. Int J Antimicrob Agents, 33: 4-7.
4. Esfandiari Z, Jalali M, Ezzatpanah H, et al (2014). Occurrence of Clostridium difficile in seasoned hamburgers and seven pro-cessing plants in Iran. BMC Microbiol, 14:283.
5. Nourbakhsh F, Tajbakhsh E (2021). Neuro-toxicity mechanism of Ochratoxin A. Qual Assur Saf Crops Foods, 13(2): 34-45.
6. Heise J, Witt P, Maneck C, et al (2021). Prevalence and phylogenetic relation-ship of Clostridioides difficile strains in fresh poultry meat samples processed in different cutting plants. Int J Food Micro-biol, 339:109032.
7. World Health Organization (2000). World Health Organization report on infec-tious diseases. Overcoming antimicrobi-al resistance https://www.who.int/teams/integrated-health-services/clinical-services-and-systems/surgical-care/infectious-diseases.
8. Waqas M, Mohib K, Saleem A, et al (2022). Rifaximin therapy for patients with met-ronidazole-unresponsive Clostridium dif-ficile infection. Infection. Cureus, 14(4): e24140.
9. Freeman J, Wilcox MH (1999). Antibiotics and Clostridium difficile. Microbes Infect, 1(5): 377−84.
10. Liberati A, Altman DG, Tetzlaff J, et al (2009). The PRISMA statement for re-porting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med, 6(7):e1000100.
11. Joanna Briggs Institute (2017). Critical Ap-praisal tools for use in JBI Systematic Reviews Checklist for Analytical Cross-Sectional Studies. https://jbi.global/critical-appraisal-tools
12. Gurevitch J, Koricheva J, Nakagawa S, et al (2018). Meta-analysis and the science of research synthesis. Nature, 555(7695):175-182.
13. Marvidis D, Salanti G (2014). How to assess publication bias: funnel plot, trim-and-fill method and selectionmodels. Evid Based Ment Health; 17(1):30.
14. Rodriguez-Palacios, Mo KQ, Shah BU, et al (2020). Global and Historical Distribu-tion of Clostridioides difficile in the human diet (1981-2019): Systematic review and meta-analysis of 21886 samples reveal sources of heterogeneity, high risk foods, and unexpected higher preva-lence toward the tropic. Front Med (Lau-sanne), 7:9.
15. Kacar A, Omuzbuken B (2017). Assessing the seawater quality of a coastal city us-ing fecal indicators and environmental variables (eastern Aegean Sea). Mar Pollut Bull, 123: 400–3.
16. McSharry S, Koolman L, Whyte P, et al (2021). Investigation of the effectiveness of disinfectants used in meat-processing facilities to control Clostridium sporogenes and Clostridioides difficile spores. Foods, 10(6):1436.
17. Smits WK, Lyras DB, Lacy DB, et al (2016). Clostridium difficile infection. Nat Rev Dis Primers, 2: 16020.
18. Mounsey A, Smith KL, Reddy VC (2020). Clostridioides difficile infection: Update on management. Am Fam Physician, 101 (3): 168-75.
19. Sholeh M, Krutova M, Forouzesh M, et al (2020). Antimicrobial resistance in Clos-tridioides (Clostridium) difficile derived from humans: a systematic review and meta-analysis. Antimicrob Resist Infect Control, 9: 158.
20. Nasiri MJ, Goudarzi M, Hajikhani B, et al (2018). Clostridioides (Clotstidium) difficile in-fection in hospitalized patients with an-tibiotic-associated diarrhea: a systematic review and meta-analysis. Anaerobe, 50: 32-7.
21. Troiano T, Harmanus C, M.J.G. Sanders I, et al (2015). Toxigenic Clostridium difficile PCR ribotypes in edible marine bivalve molluscs in Italy. Int J Food Microbiol, 208: 30-4.
22. Saha S, Kappor S, Tariq R, et al (2019). In-creasing antibiotic resistance in Clos-tridioides difficile: A systematic review and meta-analysis. Anaerobe, 58: 35-46.
23. Rodriguez C, Mith H, Taminiau B, et al (2021). First isolation of Clostridioides dif-ficile from smoked and dried freshwater fish in Cambodia. Food Control, 124: 107895.
24. Fayez M, El-Ghareeb WR, Elmoslemany A et al (2021). Genotyping and antimicro-bial susceptibility of Clostridium perfringens and Clostridioides difficile in camel minced meat. Pathogens, 10(12): 1640.
25. Licciardi C, Primavilla S, Roila R, et al (2021). Prevalence, Molecular Character-ization and antimicrobial susceptibility of Clostridioides difficile isolated from pig carcasses and pork Products in Central Italy. Int J Environ Res Public Health, 18(21): 11368.
26. Attia AET (2021). Retail chikcen meats as potential sources of Clostridioides difficile in Al-Jouf, Saudi Arabia. J Infect Dev Ctries, 15(7): 972-978.
27. Tsuchiya AC, Gomes ES, Kuaye AY, et al (2022). Detection and pathogenic poten-tial of Clostridium difficile in commercial meat and meat products in Brazil. Food Sci Technol Int, 28 (1): 85-92.
28. Nayebpour F, Rahimi E (2020). Incidence and Profiles of Antibiotic Resistance and Putative Genes of the Clostridium dif-ficile recovered from fish. Egypt J Vet Sci, 51 (3): 349-56.
29. Usui M, Maruko A, Harada M et al (2020). Prevalence and characterization of Clos-tridioides difficile isolates from retail food products (vegetables and meats) in Ja-pan. Anaerobe, 61:102132.
30. Muratoglu K, Akkaya E, Hampikyan H, et al (2020). Detection, Characterization and Antibiotic Susceptibility of Clostridioides (Clostridium) difficile in Meat Products. Food Sci Anim Resour, 40(4): 578-587.
31. Bingol EB, Hampikyan H, Muratoglu K, et al (2020). Characterization and antibiotic susceptibility profile of Clostridioides (Clos-tridium) diffiicle isolated from chicken carcasses. J Vet Res, 64(3): 407-12.
32. Agnoletti F, Arcangeli G, Barbanti F, et al (2019). Survey, characterization and an-timicrobial susceptibility of Clostridium difficile from marine bivalve shellfish of North Adriatic Sea. Int J Food Microbiol, 298: 74-80.
33. Zamani AH, Razmyar J, Berger FK, et al (2019). Isolation and toxin gene detec-tion of Clostridium (Clostridioides) difficile from traditional and commercial quail farms and packed quail meat for market supply. Acta Vet Hung, 67: 499-504.
34. Nayebpour F, Rahimi E (2019). Prevalence, antibiotic resistance, and toxigenic gene profile of the Clostridium difficile isolated from molluscan shellfish. J Food Saf, 39(1): e12586.
35. Abdel-Glil M, Thomas P, Schmoock G et al (2018). Presence of Clostridium difficile in poultry and poultry meat in Egypt. An-aerobe, 51: 21-25.
36. Lee JY, Cho YS (2018). Prevalence of Clos-tridium difficile isolated from various raw meats in Korea. Food Sci Biotechnol, 27(3):883-889.
37. Ersöz ŞŞ, Coşansu S (2018). Prevalence of Clostridium difficile isolated from beef and chicken meat products in Turkey. Korean J Food Sci Anim Resour, 38(4):759-767.
38. Bakri M (2018). Prevalence of Clostridium dif-ficile in raw cow, sheep, and goat meat in Jazan, Saudi Arabia. Saudi J Biol Sci, 25(4):783-5.
39. Pires RN, Caurio CFB, Saldanha GZ et al (2018). Clostridium difficile contamination in retail meat products in Brazil. Braz J Infect Dis, 22(4): 345-346.
40. Atasoy F, Gucukoglu A (2017). Detection of Clostridium difficile and toxin genes in samples of modified atmosphere pack-aged (MAP) minced and cubed beef meat. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 64(3):165-70.
41. Kheradmand M, Jalilian S, Alvandi A et al (2017). Prevalence of Clostridium difficile and its toxigenic genotype in beef sam-ples in west of Iran. Iran J Microbiol, 9 (3): 169-73.
42. Razmyar J, Jamshidi A, Khanzadi S, et al (2017). Toxigenic Clostridium difficile in re-tail packed chicken meat and broiler flocks in northeastern Iran. Iran J Vet Res, 18(4):271-274.
43. Mooyottu S, Flock G, Kollanoor-Johny A, et al (2015). Characterization of a multi-drug resistant C. difficile meat isolate. Int J Food Microbiol, 192:111–6.
44. Rahimi E, Khaksar F (2015). Detection of toxigenic Clostridium difficile strains isolat-ed from meat and meat products in Iran. Bulgarian J Vet Med, 18:277-81.
45. Guran HS, Ilhak OI (2015). Clostridium dif-ficile in retail chicken meat parts and liv-er in the Eastern Region of Turkey. J Verbraucherschutz und Lebensmittelsicherheit, 10(4): 359-64.
46. Esfandiari Z, Weese J, Ezzatpanah H, et al (2015). Isolation and Characterization of Clostridium difficile in Farm Animals from Slaughterhouse to Retail Stage in Isfa-han, Iran. Foodborne Pathog Dis, 12 (10): 864-6
47. Esfandiari Z, Jalali M, Ezzatpanah H, et al (2014). Prevalence and Characterization of Clostridium difficile in Beef and Mutton Meats of Isfahan Region, Iran. Jundishapur J Microbiol, 7(8): e16771.
48. Rodriguez C, Taminiau B, Avesani V, et al (2014). Multilocus sequence typing analy-sis and antibiotic resistance of Clostridi-um difficile strains isolated from retail meat and humans in Belgium. Food Mi-crobiol, 42: 166–71.
49. Rahimi E, Jalali M, Weese JS (2014). Preva-lence of Clostridium difficile in raw beef, cow, sheep, goat, camel and buffalo meat in Iran. BMC Public Health, 14: 119.
50. Kouassi KA, Dadie AT, N’Guessan KF, et al (2014). Clostridium perfringens and Clos-tridium difficile in cooked beef sold in Côte d’lvoire and their antimicrobial susceptibility. Anaerobe, 28:90-4.
51. Varshney JB, Very KJ, Williams JL, et al (2014). Characterization of Clostridium dif-ficile isolates from human fecal samples and retail meat from Pennsylvania. Foodborne Pathog Dis, 11(10): 822-9.
52. Norman KN, Harveyb RB, Andrewsb K, et al (2014). Survey of Clostridium difficile in retail seafood in College Station, Texas. Food Addit Contam Part A Chem Anal Con-trol Expo Risk Assess, 31(6): 1127–9.
53. Quesada-Gómez C, Mulvey MR, Vargas P, et al (2013). Isolation of a toxigenic and clinical genotype of Clostridium difficile in retail meats in Costa Rica. J Food Prot, 76(2):348-51.
54. Kalchayanand N, Arthur TM, Bosilevac JM, et al (2013). Isolation and characteriza-tion of Clostridium difficile associated with beef cattle and commercially produced ground beef. J Food Prot, 76(2): 256-64.
55. Hasanzadeh A, Rahimi E (2013). Isolation of Clostridium difficile from chicken meat sold in meat stores of Isfahan City. Adv Environ Biol, 7(9):2372-5.
56. Hasanzade A, Rahimi E (2013). Isolation of Clostridium Difficile from Turkey and Os-trich Meat Sold in Meat Stores if Isfahan City. Int J Adv Biol Biom Res, 1(9):963-7.
57. Curry SR, Marsh JW, Schlackman JL et al (2012). Prevalence of Clostridium difficile in uncooked ground meat products from Pittsburgh, Pennsylvania. Appl Environ Microbiol, 78(12): 4183–6.
58. Limbago B, Thompson AD, Greene SA, et al (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 Microbiol, 32: 448-51.
59. Visser M, Sepehrim S, Olson N, et al (2012). Detection of Clostridium difficile in retail ground meat products in Manotoba. Can J Infect Dis Med Microbiol, 23(1): 28-30.
60. Houser BA, Soehnlen MK, Wolfgang DR, et al (2012). Prevalence of Clostridium dif-ficile toxin genes in the feces of veal calves and incidence of ground veal contamination. Foodborne Pathog Dis, 9(1):32-6.
61. Pasquale V, Romano VJ, Rupnik M, et al (2011). Isolation and characterization of Clostridium difficile from shellfish and ma-rine environments. Folia Microbiol (Praha), 56(5): 431–7.
62. Pasquale V, Romano V, Rupnik M, et al (2012). Occurrence of toxigenic Clostridi-um difficile in edible bivalve molluscs. Food Microbiol, 31(2): 309–12.
63. Metcalf D, Avery BP, Janecko N, et al (2011). Clostridium difficile in seafood and fish. Anaerobe, 17:85-6.
64. De Boer E, Zwartkruis-Nahuis A, Heuvelink AE, et al (2011). Prevalence of Clostridium difficile in retailed meat in the Nether-lands. Int J Food Microbiol, 144: 561-4.
65. Metcalf D, Reid-Smith RJ, Avery BP, et al (2010). Prevalence of Clostridium difficile in retail pork. Can Vet J, 51(8):873–6.
66. Hoffer E, Haechler H, Frei R, et al (2010). Low occurrence of Clostridium difficile in fecal samples of healthy calves and pigs at slaughter and in minced meat in Swit-zerland. J Food Prot, 73(5): 973-5.
67. Bouttier S, Barc MC, Felix B, et al (2010). Clostridium difficile in Ground Meat, France. Emerg Infect Dis, 16 (4):733-5.
68. Weese JS, Reid-Smith RJ, Avery BP, et al (2010). Detection and characterization of Clostridium difficile in retail chicken. Lett Appl Microbiol, 50(4):362-5.
69. Weese JS, Avery BP, Rousseau J, et al (2009). Detection and enumeration of Clostidi-um difficile spores in retail beef and pork. Applied Environ Microbiol, 75 (15): 5009-11.
70. Indra A, Lassing H, Baliko N, et al (2009). Clostridium difficile: a new zoonotic agent? Wien Klin Wochenschr, 121(3-4): 91-5.
71. Songer JG, Trinh HT, Killgore GE, et al (2009). Clostridium difficile in retail meat products, USA, 2007. Emerg Infect Dis, 15(5):819-21.
72. Von Abercron, SM, Karlsson F, Wigh GT, et al (2009). Low occurrence of Clostridi-um difficile in retail ground meat in Swe-den. J Food Prot, 72(8): 1732-4.
73. Rodriguez-Palacios A, Staempfli HR, Duf-field T, et al (2007). Clostridium difficile in retail ground meat, Canada. Emerg Infect Dis,13(3): 485–7.
2. Lawson PA, Citron DM, Tyrrell KL, et al (2016). Reclassification of Clostridium dif-ficile as Clostridioides difficile (Hall and O'Toole 1935) Prevot 1938. Anaerobe, 40: 95-9.
3. Weiss K (2009). Toxin binding treatment for clostridium difficile: a review including reports of studies with tolevamer. Int J Antimicrob Agents, 33: 4-7.
4. Esfandiari Z, Jalali M, Ezzatpanah H, et al (2014). Occurrence of Clostridium difficile in seasoned hamburgers and seven pro-cessing plants in Iran. BMC Microbiol, 14:283.
5. Nourbakhsh F, Tajbakhsh E (2021). Neuro-toxicity mechanism of Ochratoxin A. Qual Assur Saf Crops Foods, 13(2): 34-45.
6. Heise J, Witt P, Maneck C, et al (2021). Prevalence and phylogenetic relation-ship of Clostridioides difficile strains in fresh poultry meat samples processed in different cutting plants. Int J Food Micro-biol, 339:109032.
7. World Health Organization (2000). World Health Organization report on infec-tious diseases. Overcoming antimicrobi-al resistance https://www.who.int/teams/integrated-health-services/clinical-services-and-systems/surgical-care/infectious-diseases.
8. Waqas M, Mohib K, Saleem A, et al (2022). Rifaximin therapy for patients with met-ronidazole-unresponsive Clostridium dif-ficile infection. Infection. Cureus, 14(4): e24140.
9. Freeman J, Wilcox MH (1999). Antibiotics and Clostridium difficile. Microbes Infect, 1(5): 377−84.
10. Liberati A, Altman DG, Tetzlaff J, et al (2009). The PRISMA statement for re-porting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med, 6(7):e1000100.
11. Joanna Briggs Institute (2017). Critical Ap-praisal tools for use in JBI Systematic Reviews Checklist for Analytical Cross-Sectional Studies. https://jbi.global/critical-appraisal-tools
12. Gurevitch J, Koricheva J, Nakagawa S, et al (2018). Meta-analysis and the science of research synthesis. Nature, 555(7695):175-182.
13. Marvidis D, Salanti G (2014). How to assess publication bias: funnel plot, trim-and-fill method and selectionmodels. Evid Based Ment Health; 17(1):30.
14. Rodriguez-Palacios, Mo KQ, Shah BU, et al (2020). Global and Historical Distribu-tion of Clostridioides difficile in the human diet (1981-2019): Systematic review and meta-analysis of 21886 samples reveal sources of heterogeneity, high risk foods, and unexpected higher preva-lence toward the tropic. Front Med (Lau-sanne), 7:9.
15. Kacar A, Omuzbuken B (2017). Assessing the seawater quality of a coastal city us-ing fecal indicators and environmental variables (eastern Aegean Sea). Mar Pollut Bull, 123: 400–3.
16. McSharry S, Koolman L, Whyte P, et al (2021). Investigation of the effectiveness of disinfectants used in meat-processing facilities to control Clostridium sporogenes and Clostridioides difficile spores. Foods, 10(6):1436.
17. Smits WK, Lyras DB, Lacy DB, et al (2016). Clostridium difficile infection. Nat Rev Dis Primers, 2: 16020.
18. Mounsey A, Smith KL, Reddy VC (2020). Clostridioides difficile infection: Update on management. Am Fam Physician, 101 (3): 168-75.
19. Sholeh M, Krutova M, Forouzesh M, et al (2020). Antimicrobial resistance in Clos-tridioides (Clostridium) difficile derived from humans: a systematic review and meta-analysis. Antimicrob Resist Infect Control, 9: 158.
20. Nasiri MJ, Goudarzi M, Hajikhani B, et al (2018). Clostridioides (Clotstidium) difficile in-fection in hospitalized patients with an-tibiotic-associated diarrhea: a systematic review and meta-analysis. Anaerobe, 50: 32-7.
21. Troiano T, Harmanus C, M.J.G. Sanders I, et al (2015). Toxigenic Clostridium difficile PCR ribotypes in edible marine bivalve molluscs in Italy. Int J Food Microbiol, 208: 30-4.
22. Saha S, Kappor S, Tariq R, et al (2019). In-creasing antibiotic resistance in Clos-tridioides difficile: A systematic review and meta-analysis. Anaerobe, 58: 35-46.
23. Rodriguez C, Mith H, Taminiau B, et al (2021). First isolation of Clostridioides dif-ficile from smoked and dried freshwater fish in Cambodia. Food Control, 124: 107895.
24. Fayez M, El-Ghareeb WR, Elmoslemany A et al (2021). Genotyping and antimicro-bial susceptibility of Clostridium perfringens and Clostridioides difficile in camel minced meat. Pathogens, 10(12): 1640.
25. Licciardi C, Primavilla S, Roila R, et al (2021). Prevalence, Molecular Character-ization and antimicrobial susceptibility of Clostridioides difficile isolated from pig carcasses and pork Products in Central Italy. Int J Environ Res Public Health, 18(21): 11368.
26. Attia AET (2021). Retail chikcen meats as potential sources of Clostridioides difficile in Al-Jouf, Saudi Arabia. J Infect Dev Ctries, 15(7): 972-978.
27. Tsuchiya AC, Gomes ES, Kuaye AY, et al (2022). Detection and pathogenic poten-tial of Clostridium difficile in commercial meat and meat products in Brazil. Food Sci Technol Int, 28 (1): 85-92.
28. Nayebpour F, Rahimi E (2020). Incidence and Profiles of Antibiotic Resistance and Putative Genes of the Clostridium dif-ficile recovered from fish. Egypt J Vet Sci, 51 (3): 349-56.
29. Usui M, Maruko A, Harada M et al (2020). Prevalence and characterization of Clos-tridioides difficile isolates from retail food products (vegetables and meats) in Ja-pan. Anaerobe, 61:102132.
30. Muratoglu K, Akkaya E, Hampikyan H, et al (2020). Detection, Characterization and Antibiotic Susceptibility of Clostridioides (Clostridium) difficile in Meat Products. Food Sci Anim Resour, 40(4): 578-587.
31. Bingol EB, Hampikyan H, Muratoglu K, et al (2020). Characterization and antibiotic susceptibility profile of Clostridioides (Clos-tridium) diffiicle isolated from chicken carcasses. J Vet Res, 64(3): 407-12.
32. Agnoletti F, Arcangeli G, Barbanti F, et al (2019). Survey, characterization and an-timicrobial susceptibility of Clostridium difficile from marine bivalve shellfish of North Adriatic Sea. Int J Food Microbiol, 298: 74-80.
33. Zamani AH, Razmyar J, Berger FK, et al (2019). Isolation and toxin gene detec-tion of Clostridium (Clostridioides) difficile from traditional and commercial quail farms and packed quail meat for market supply. Acta Vet Hung, 67: 499-504.
34. Nayebpour F, Rahimi E (2019). Prevalence, antibiotic resistance, and toxigenic gene profile of the Clostridium difficile isolated from molluscan shellfish. J Food Saf, 39(1): e12586.
35. Abdel-Glil M, Thomas P, Schmoock G et al (2018). Presence of Clostridium difficile in poultry and poultry meat in Egypt. An-aerobe, 51: 21-25.
36. Lee JY, Cho YS (2018). Prevalence of Clos-tridium difficile isolated from various raw meats in Korea. Food Sci Biotechnol, 27(3):883-889.
37. Ersöz ŞŞ, Coşansu S (2018). Prevalence of Clostridium difficile isolated from beef and chicken meat products in Turkey. Korean J Food Sci Anim Resour, 38(4):759-767.
38. Bakri M (2018). Prevalence of Clostridium dif-ficile in raw cow, sheep, and goat meat in Jazan, Saudi Arabia. Saudi J Biol Sci, 25(4):783-5.
39. Pires RN, Caurio CFB, Saldanha GZ et al (2018). Clostridium difficile contamination in retail meat products in Brazil. Braz J Infect Dis, 22(4): 345-346.
40. Atasoy F, Gucukoglu A (2017). Detection of Clostridium difficile and toxin genes in samples of modified atmosphere pack-aged (MAP) minced and cubed beef meat. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 64(3):165-70.
41. Kheradmand M, Jalilian S, Alvandi A et al (2017). Prevalence of Clostridium difficile and its toxigenic genotype in beef sam-ples in west of Iran. Iran J Microbiol, 9 (3): 169-73.
42. Razmyar J, Jamshidi A, Khanzadi S, et al (2017). Toxigenic Clostridium difficile in re-tail packed chicken meat and broiler flocks in northeastern Iran. Iran J Vet Res, 18(4):271-274.
43. Mooyottu S, Flock G, Kollanoor-Johny A, et al (2015). Characterization of a multi-drug resistant C. difficile meat isolate. Int J Food Microbiol, 192:111–6.
44. Rahimi E, Khaksar F (2015). Detection of toxigenic Clostridium difficile strains isolat-ed from meat and meat products in Iran. Bulgarian J Vet Med, 18:277-81.
45. Guran HS, Ilhak OI (2015). Clostridium dif-ficile in retail chicken meat parts and liv-er in the Eastern Region of Turkey. J Verbraucherschutz und Lebensmittelsicherheit, 10(4): 359-64.
46. Esfandiari Z, Weese J, Ezzatpanah H, et al (2015). Isolation and Characterization of Clostridium difficile in Farm Animals from Slaughterhouse to Retail Stage in Isfa-han, Iran. Foodborne Pathog Dis, 12 (10): 864-6
47. Esfandiari Z, Jalali M, Ezzatpanah H, et al (2014). Prevalence and Characterization of Clostridium difficile in Beef and Mutton Meats of Isfahan Region, Iran. Jundishapur J Microbiol, 7(8): e16771.
48. Rodriguez C, Taminiau B, Avesani V, et al (2014). Multilocus sequence typing analy-sis and antibiotic resistance of Clostridi-um difficile strains isolated from retail meat and humans in Belgium. Food Mi-crobiol, 42: 166–71.
49. Rahimi E, Jalali M, Weese JS (2014). Preva-lence of Clostridium difficile in raw beef, cow, sheep, goat, camel and buffalo meat in Iran. BMC Public Health, 14: 119.
50. Kouassi KA, Dadie AT, N’Guessan KF, et al (2014). Clostridium perfringens and Clos-tridium difficile in cooked beef sold in Côte d’lvoire and their antimicrobial susceptibility. Anaerobe, 28:90-4.
51. Varshney JB, Very KJ, Williams JL, et al (2014). Characterization of Clostridium dif-ficile isolates from human fecal samples and retail meat from Pennsylvania. Foodborne Pathog Dis, 11(10): 822-9.
52. Norman KN, Harveyb RB, Andrewsb K, et al (2014). Survey of Clostridium difficile in retail seafood in College Station, Texas. Food Addit Contam Part A Chem Anal Con-trol Expo Risk Assess, 31(6): 1127–9.
53. Quesada-Gómez C, Mulvey MR, Vargas P, et al (2013). Isolation of a toxigenic and clinical genotype of Clostridium difficile in retail meats in Costa Rica. J Food Prot, 76(2):348-51.
54. Kalchayanand N, Arthur TM, Bosilevac JM, et al (2013). Isolation and characteriza-tion of Clostridium difficile associated with beef cattle and commercially produced ground beef. J Food Prot, 76(2): 256-64.
55. Hasanzadeh A, Rahimi E (2013). Isolation of Clostridium difficile from chicken meat sold in meat stores of Isfahan City. Adv Environ Biol, 7(9):2372-5.
56. Hasanzade A, Rahimi E (2013). Isolation of Clostridium Difficile from Turkey and Os-trich Meat Sold in Meat Stores if Isfahan City. Int J Adv Biol Biom Res, 1(9):963-7.
57. Curry SR, Marsh JW, Schlackman JL et al (2012). Prevalence of Clostridium difficile in uncooked ground meat products from Pittsburgh, Pennsylvania. Appl Environ Microbiol, 78(12): 4183–6.
58. Limbago B, Thompson AD, Greene SA, et al (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 Microbiol, 32: 448-51.
59. Visser M, Sepehrim S, Olson N, et al (2012). Detection of Clostridium difficile in retail ground meat products in Manotoba. Can J Infect Dis Med Microbiol, 23(1): 28-30.
60. Houser BA, Soehnlen MK, Wolfgang DR, et al (2012). Prevalence of Clostridium dif-ficile toxin genes in the feces of veal calves and incidence of ground veal contamination. Foodborne Pathog Dis, 9(1):32-6.
61. Pasquale V, Romano VJ, Rupnik M, et al (2011). Isolation and characterization of Clostridium difficile from shellfish and ma-rine environments. Folia Microbiol (Praha), 56(5): 431–7.
62. Pasquale V, Romano V, Rupnik M, et al (2012). Occurrence of toxigenic Clostridi-um difficile in edible bivalve molluscs. Food Microbiol, 31(2): 309–12.
63. Metcalf D, Avery BP, Janecko N, et al (2011). Clostridium difficile in seafood and fish. Anaerobe, 17:85-6.
64. De Boer E, Zwartkruis-Nahuis A, Heuvelink AE, et al (2011). Prevalence of Clostridium difficile in retailed meat in the Nether-lands. Int J Food Microbiol, 144: 561-4.
65. Metcalf D, Reid-Smith RJ, Avery BP, et al (2010). Prevalence of Clostridium difficile in retail pork. Can Vet J, 51(8):873–6.
66. Hoffer E, Haechler H, Frei R, et al (2010). Low occurrence of Clostridium difficile in fecal samples of healthy calves and pigs at slaughter and in minced meat in Swit-zerland. J Food Prot, 73(5): 973-5.
67. Bouttier S, Barc MC, Felix B, et al (2010). Clostridium difficile in Ground Meat, France. Emerg Infect Dis, 16 (4):733-5.
68. Weese JS, Reid-Smith RJ, Avery BP, et al (2010). Detection and characterization of Clostridium difficile in retail chicken. Lett Appl Microbiol, 50(4):362-5.
69. Weese JS, Avery BP, Rousseau J, et al (2009). Detection and enumeration of Clostidi-um difficile spores in retail beef and pork. Applied Environ Microbiol, 75 (15): 5009-11.
70. Indra A, Lassing H, Baliko N, et al (2009). Clostridium difficile: a new zoonotic agent? Wien Klin Wochenschr, 121(3-4): 91-5.
71. Songer JG, Trinh HT, Killgore GE, et al (2009). Clostridium difficile in retail meat products, USA, 2007. Emerg Infect Dis, 15(5):819-21.
72. Von Abercron, SM, Karlsson F, Wigh GT, et al (2009). Low occurrence of Clostridi-um difficile in retail ground meat in Swe-den. J Food Prot, 72(8): 1732-4.
73. Rodriguez-Palacios A, Staempfli HR, Duf-field T, et al (2007). Clostridium difficile in retail ground meat, Canada. Emerg Infect Dis,13(3): 485–7.
| Files | ||
| Issue | Vol 52 No 12 (2023) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v52i12.14313 | |
| Keywords | ||
| Clostridioides difficile Meat Antibiotic resistance Systematic review Meta-analysis | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Esfandiari Z, Shoaei P, Vakili B, Farajzadegan Z, Tarrahi MJ, Emami Z, Fakhri Y, Weese JS, Mahmudiono T. Prevalence and Antibiotic Resistance of Clostridioides (Clostridium difficile) In Meat and Meat Products: A Systematic Review and Meta-Analysis. Iran J Public Health. 2023;52(12):2516-2527.
