Citation: Joana Barbosa, Ana Campos, Paula Teixeira. Methods currently applied to study the prevalence of Clostridioides difficile in foods[J]. AIMS Agriculture and Food, 2020, 5(1): 102-128. doi: 10.3934/agrfood.2020.1.102
[1] | Lawson PA, Citron DM, Tyrrell KL, et al. (2016) Reclassification of Clostridium difficile as Clostridioides difficile (Hall and O'Toole 1935) Prevot 1938. Anaerobe 40: 95-99. doi: 10.1016/j.anaerobe.2016.06.008 |
[2] | Smits WK, Lyras D, Lacy DB, et al. (2016) Clostridium difficile infection. Nat Rev Dis Prim 2: 1-20. |
[3] | Kilic A, Alam MJ, Tisdel NL, et al. (2015) Multiplex real-time PCR method for simultaneous identification and toxigenic type characterization of Clostridium difficile from stool samples. Ann Lab Med 35: 306-313. doi: 10.3343/alm.2015.35.3.306 |
[4] | McDonald LC, Killgore GE, Thompson A, et al. (2005) An epidemic, toxin gene-variant strain of Clostridium difficile. N Engl J Med 353: 2433-2441. doi: 10.1056/NEJMoa051590 |
[5] | DePestel DD, Aronoff DM (2013) Epidemiology of Clostridium difficile infection. J Pharm Pract 26: 464-475. doi: 10.1177/0897190013499521 |
[6] | Weese JS, Avery BP, Rousseau J, et al. (2009) Detection and enumeration of Clostridium difficile spores in retail beef and pork. Appl Environ Microbiol 75: 5009-5011. doi: 10.1128/AEM.00480-09 |
[7] | Wu YC, Chen CM, Kuo CJ, et al. (2017) Prevalence and molecular characterization of Clostridium difficile isolates from a pig slaughterhouse, pork, and humans in Taiwan. Int J Food Microbiol 242: 37-44. doi: 10.1016/j.ijfoodmicro.2016.11.010 |
[8] | Songer JG, Trinh HT, Killgore GE, et al. (2009) Clostridium difficile in retail meat products, USA, 2007. Emerg Infect Dis 15: 819-821. doi: 10.3201/eid1505.081071 |
[9] | Weese JS, Reid-Smith RJ, Avery BP, et al. (2010) Detection and characterization of Clostridium difficile in retail chicken. Lett Appl Microbiol 50: 362-365. doi: 10.1111/j.1472-765X.2010.02802.x |
[10] | Harvey RB, Norman KN, Andrews K, et al. (2011) Clostridium difficile in poultry and poultry meat. Foodborne Pathog Dis 8: 1321-1323. doi: 10.1089/fpd.2011.0936 |
[11] | Romano V, Pasquale V, Lemee L, et al. (2018) Clostridioides difficile in the environment, food, animals and humans in southern Italy: Occurrence and genetic relatedness. Comp Immunol Microbiol Infect Dis 59: 41-46. doi: 10.1016/j.cimid.2018.08.006 |
[12] | Bakri MM, Brown DJ, Butcher JP, et al. (2009) Clostridium difficile in ready-to-eat salads, scotland. Emerg Infect Dis 15: 817-818. doi: 10.3201/eid1505.081186 |
[13] | Yamoudy M, Mirlohi M, Isfahani BN, et al. (2015) Isolation of toxigenic Clostridium difficile from ready-to-eat salads by multiplex polymerase chain reaction in Isfahan, Iran. Adv Biomed Res 4: 87. doi: 10.4103/2277-9175.156650 |
[14] | Metcalf DS, Costa MC, Dew WMV, et al. (2010) Clostridium difficile in vegetables, Canada. Lett Appl Microbiol 51: 600-602. doi: 10.1111/j.1472-765X.2010.02933.x |
[15] | 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. doi: 10.1099/jmm.0.056358-0 |
[16] | Han Y (2016) Detection of antibiotic resistance Clostridium difficile in lettuce. Master thesis, Louisiana State University. |
[17] | Rodriguez-Palacios A, Ilic S, LeJeune JT (2014) Clostridium difficile with moxifloxacin/clindamycin resistance in vegetables in Ohio, USA, and prevalence meta-analysis. J Pathog: 158601. |
[18] | Troiano T, Harmanus C, Sanders IMJG, et al. (2015) Toxigenic Clostridium difficile PCR ribotypes in edible marine bivalve molluscs in Italy. Int J Food Microbiol 208: 30-34. doi: 10.1016/j.ijfoodmicro.2015.05.002 |
[19] | Norman KN, Harvey RB, Andrews K, et al. (2014) Survey of Clostridium difficile in retail seafood in College Station, Texas. Food Addit Contam A 31: 1127-1129. doi: 10.1080/19440049.2014.888785 |
[20] | Metcalf D, Avery BP, Janecko N, et al. (2011) Clostridium difficile in seafood and fish. Anaerobe 17: 85-86. doi: 10.1016/j.anaerobe.2011.02.008 |
[21] | Rupnik M (2007) Is Clostridium difficile-associated infection a potentially zoonotic and foodborne disease? Clin Microbiol Infect 13: 457-459. doi: 10.1111/j.1469-0691.2007.01687.x |
[22] | Warriner K, Xu C, Habash M, et al. (2017) Dissemination of Clostridium difficile in food and the environment: Significant sources of C. difficile community-acquired infection? J Appl Microbiol 122: 542-553. |
[23] | Pasquale V, Romano VJ, Rupnik M, et al. (2011) Isolation and characterization of Clostridium difficile from shellfish and marine environments. Folia Microbiol (Praha) 56: 431-437. doi: 10.1007/s12223-011-0068-3 |
[24] | Xu C, Salsali H, Weese S, et al. (2015) Inactivation of Clostridium difficile in sewage sludge by anaerobic thermophilic digestion. Can J Microbiol 62: 13-26. |
[25] | Romano V, Pasquale V, Krovacek K, et al. (2012) Toxigenic Clostridium difficile PCR Ribotypes from wastewater treatment plants in southern Switzerland. App Environ Microbiol 78: 6643-6646. doi: 10.1128/AEM.01379-12 |
[26] | Bakri M (2018) Prevalence of Clostridium difficile in raw cow, sheep, and goat meat in Jazan, Saudi Arabia. Saudi J Biol Sci 25: 783-785. doi: 10.1016/j.sjbs.2016.07.002 |
[27] | Rodriguez C, Taminiau B, Avesani V, et al. (2014) Multilocus sequence typing analysis and antibiotic resistance of Clostridium difficile strains isolated from retail meat and humans in Belgium. Food Microbiol 42: 166-171. doi: 10.1016/j.fm.2014.03.021 |
[28] | Varshney JB, Very KJ, Williams JL, et al. (2014) Characterization of Clostridium difficile isolates from human fecal samples and retail meat from Pennsylvania. Foodborne Pathog Dis 11: 822-829. doi: 10.1089/fpd.2014.1790 |
[29] | Lim SC, Foster NF, Riley TV (2016) Susceptibility of Clostridium difficile to the food preservatives sodium nitrite, sodium nitrate and sodium metabisulphite. Anaerobe 37: 67-71. doi: 10.1016/j.anaerobe.2015.12.004 |
[30] | 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: 4183-4186. doi: 10.1128/AEM.00842-12 |
[31] | 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: 1-5. |
[32] | 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: 448-451. doi: 10.1016/j.fm.2012.08.005 |
[33] | Abdel-Glil MY, Thomas P, Schmoock G, et al. (2018) Presence of Clostridium difficile in poultry and poultry meat in Egypt. Anaerobe 51: 21-25. doi: 10.1016/j.anaerobe.2018.03.009 |
[34] | Guran HS, Ilhak OI (2015) Clostridium difficile in retail chicken meat parts and liver in the Eastern Region of Turkey. J Verbrauch Lebensm 10: 359-364. doi: 10.1007/s00003-015-0950-z |
[35] | Razmyar J, Jamshidi A, Khanzadi S, et al. (2017) Toxigenic Clostridium difficile in retail packed chicken meat and broiler flocks in northeastern Iran. Iran. J Vet Res 18: 271-274. |
[36] | Lee JY, Lee DY, Cho YS (2018) Prevalence of Clostridium difficile isolated from various raw meats in Korea. Food Sci Biotechnol 27: 883-889. doi: 10.1007/s10068-018-0318-0 |
[37] | Ersöz ŞŞ, Coşansu S (2018) Prevalence of Clostridium difficile isolated from beef and chicken meat products in Turkey. Korean J Food Sci An 38: 759-767. |
[38] | Mooyottu S, Flock G, Kollanoor-Johny A, et al. (2015) Characterization of a multidrug resistant C. difficile meat isolate. Int J Food Microbiol 192: 111-116. doi: 10.1016/j.ijfoodmicro.2014.10.002 |
[39] | Quesada-Gomez 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 Protect 76: 348-351. doi: 10.4315/0362-028X.JFP-12-169 |
[40] | Indra A, Lassnig H, Baliko N, et al. (2009) Clostridium difficile: a new zoonotic agent? Wiener Klinische Wochenschrift 121: 91-95. doi: 10.1007/s00508-008-1127-x |
[41] | De Boer E, Zwartkruis-Nahuis A, Heuvelink AE, et al. (2011) Prevalence of Clostridium difficile in retailed meat in The Netherlands. Int J Food Microbiol 144: 561-564. doi: 10.1016/j.ijfoodmicro.2010.11.007 |
[42] | Carvalho P, Barbosa J, Teixeira P (2019) Are indeed meats sold in Portugal without Clostridioides difficile? Acta Aliment 48: 391-395. doi: 10.1556/066.2019.48.3.15 |
[43] | Pires RN, Caurioa CFB, Saldanha GZ, et al. (2018) Clostridium difficile contamination in retail meat products in Brazil. Braz J Infect Dis 2018. |
[44] | Harvey RB, Norman KN, Andrews K, et al. (2011) Clostridium difficile in retail meat and processing plants in Texas. J Vet Diagn Invest 23: 8 807-811. |
[45] | Shaughnessy MK, Snider T, Sepulbeda R, et al. (2018) Prevalence and molecular characteristics of Clostridium difficile in retail meats, food-producing and companion animals, and humans in Minnesota. J Food Protect 81: 1635-1642. doi: 10.4315/0362-028X.JFP-18-104 |
[46] | Von Abercron SM, Karlsson F, Wigh GT, et al. (2009) Low occurrence of Clostridium difficile in retail ground meat in Sweden. J Food Protect 72: 1732-1734. doi: 10.4315/0362-028X-72.8.1732 |
[47] | Metcalf D, Reid-Smith RJ, Avery BP, et al. (2010) Prevalence of Clostridium difficile in retail pork. Can Vet J 51: 873-876. |
[48] | Kalchayanand N, Arthur TM, Bosilevac JM, et al. (2013) Isolation and characterization of Clostridium difficile associated with beef cattle and commercially produced ground beef. J Food Prot 76: 256-264. doi: 10.4315/0362-028X.JFP-12-261 |
[49] | Rodriguez-Palacios A, Staempfli HR, Duffield T, et al. (2007) Clostridium difficile in retail ground meat, Canada. Emerg Infect Dis 13: 485-487. doi: 10.3201/eid1303.060988 |
[50] | Esfandiari Z, Weese S, Ezzatpanah H (2014) Occurrence of Clostridium difficile in seasoned hamburgers and seven processing plants in Iran. BMC Microbiol 14: 283. doi: 10.1186/s12866-014-0283-6 |
[51] | Hofer 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 Switzerland. J Food Protect 73: 973-975. doi: 10.4315/0362-028X-73.5.973 |
[52] | Jöbstl M, Heuberger S, Indra A, et al. (2010) Clostridium difficile in raw products of animal origin. Int J Food Microbiol 138: 172-175. doi: 10.1016/j.ijfoodmicro.2009.12.022 |
[53] | Visser M, Sepehrim S, Olson N, et al. (2012) Detection of Clostridium difficile in retail ground meat products in Manitoba. Can J Infect Dis Med Microbiol 23: 28-30. doi: 10.1155/2012/646981 |
[54] | Bouttier S, Barc M-C, Felix B, et al. (2010) Clostridium difficile in ground meat, France. Emerg Infect Dis 16: 733-735. doi: 10.3201/eid1604.091138 |
[55] | Rodriguez-Palacios A, Reid-Smith RJ, Staempfli HR, et al. (2009) Possible seasonality of Clostridium difficile in retail meat, Canada. Emerg Infect Dis 15: 802-805. doi: 10.3201/eid1505.081084 |
[56] | 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. doi: 10.1186/1471-2458-14-119 |
[57] | Houser BA, Soehnlen MK, Wolfgang DR, et al. (2012) Prevalence of Clostridium difficile toxin genes in the feces of veal calves and incidence of ground veal contamination. Foodborne Pathog Dis 9: 32-36. doi: 10.1089/fpd.2011.0955 |
[58] | Kouassi KA, Dadie AT, N'Guessan KF, et al. (2014) Clostridium perfringens and Clostridium difficile in cooked beef sold in Côte d'Ivoire and their antimicrobial susceptibility. Anaerobe 28: 90-94. doi: 10.1016/j.anaerobe.2014.05.012 |
[59] | Pasquale V, Romano V, Rupnik M, et al. (2012) Occurrence of toxigenic Clostridium difficile in edible bivalve molluscs. Food Microbiol 31: 309-312. doi: 10.1016/j.fm.2012.03.001 |
[60] | Al Saif N, Brazier JS (1996) The distribution of Clostridium difficile in the environment of South Wales. J Med Microbiol 45: 133-137. doi: 10.1099/00222615-45-2-133 |
[61] | Lim SC, Foster NF, Elliott B, et al. (2018) High prevalence of Clostridium difficile on retail root vegetables, Western Australia. J Appl Microbiol 124: 585-590. doi: 10.1111/jam.13653 |
[62] | Tkalec V, Janezic S, Skik B, et al. (2019) High Clostridium difficile contamination rates of domestic and imported potatoes compared to some other vegetables in Slovenia. Food Microbiol 78: 194-200. doi: 10.1016/j.fm.2018.10.017 |
[63] | 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: 128-131. doi: 10.1016/S2221-1691(15)30156-8 |
[64] | Rodriguez C, Korsak N, Taminiau B, et al. (2015) Clostridium difficile from food and surface samples in a Belgian nursing home: An unlikely source of contamination. Anaerobe 32: 87-89. doi: 10.1016/j.anaerobe.2015.01.001 |
[65] | Aspinall ST, Hutchinson DN (1992) New selective medium for isolating Clostridium difficile from faeces. J Clin Pathol 45: 812-814. doi: 10.1136/jcp.45.9.812 |
[66] | Delmée M, Vandercam B, Avesani V, et al. (1987) Epidemiology and prevention of Clostridium difficile infections in a leukemia unit. Eur J Clin Microbiol 6: 623-627. doi: 10.1007/BF02013056 |
[67] | GeorgeWL, Sutter VL, Citron D (1979) Selective and differential medium for isolation of selective and differential medium for isolation of Clostridium difficile. J Clin Microbiol 9: 214-219. |
[68] | Marler LM, Siders JA, Wolters LC, et al. (1992) Comparison of five cultural procedures for isolation of Clostridium difficile from stools. J Clin Microbiol 30: 514-516. doi: 10.1128/JCM.30.2.514-516.1992 |
[69] | Tyrrell KL, Citron DM, Leoncio ES, et al. (2013) Evaluation of cycloserine-cefoxitin fructose agar (CCFA), CCFA with horse blood and taurocholate, and cycloserine-cefoxitin mannitol broth with taurocholate and lysozyme for recovery of Clostridium difficile isolates from fecal samples. J Clin Microbiol 51: 3094-3096. doi: 10.1128/JCM.00879-13 |
[70] | Lister M, Stevenson E, Heeg D, et al. (2014) Comparison of culture based methods for the isolation of Clostridium difficile from stool samples in a research setting. Anaerobe 28: 226-229. doi: 10.1016/j.anaerobe.2014.07.003 |
[71] | Edwards AN, Suárez JM, McBride SM (2013) Culturing and maintaining Clostridium difficile in an anaerobic environment. J Vis Exp 79: 1-8. |
[72] | Chai C, Lee KS, Lee D, et al. (2015) Non-selective and selective enrichment media for the recovery of Clostridium difficile from chopped beef. J Microbiol Methods 109: 20-24. doi: 10.1016/j.mimet.2014.12.001 |
[73] | Wilkins TD, Lyerly DM (2003) Clostridium difficile testing after 20 years, still challenging. J Clin Microbiol 41: 531-534. doi: 10.1128/JCM.41.2.531-534.2003 |
[74] | Steensels D, Verhaegen J, Lagrou K (2011) Matrix-assisted laser desorption ionization-time of flight mass spectrometry for the identification of bacteria and yeasts in a clinical microbiological laboratory: A review. Acta Clin Belg 66: 267-273. |
[75] | Reil M, Erhard M, Kuijper EJ, et al. (2011) Recognition of Clostridium difficile PCR-ribotypes 001, 027 and 126/078 using an extended MALDI-TOF MS system. Eur J Clin Microbiol Infect Dis 30: 1431-1436. doi: 10.1007/s10096-011-1238-6 |
[76] | Burnham CAD, Carroll KC (2013) Diagnosis of Clostridium difficile infection: An ongoing conundrum for clinicians and for clinical laboratories. Clin Microbiol Rev 26: 604-630. doi: 10.1128/CMR.00016-13 |
[77] | Lyerly DM, Krivan HC, Wilkins TD (1988) Clostridium difficile: its disease and toxins. Clin Microbiol Rev 1: 1-18. doi: 10.1128/CMR.1.1.1 |
[78] | Chapin KC, Dickenson RA, Wu F, et al. (2011) Comparison of five assays for detection of Clostridium difficile toxin. J Mol Diagn 13: 395-400. doi: 10.1016/j.jmoldx.2011.03.004 |
[79] | Antikainen J, Pasanen T, Mero S, et al. (2009) Detection of virulence genes of Clostridium difficile by multiplex PCR. Acta Pathol Microbiol Immunol Scand 117: 607-613. doi: 10.1111/j.1600-0463.2009.02509.x |
[80] | Kato H, Kato N, Katow S, et al. (1999) Deletions in the repeating sequences of the toxin A gene of toxin A-negative, toxin B-positive Clostridium difficile strains. FEMS Microbiol Lett 175: 197-203. doi: 10.1111/j.1574-6968.1999.tb13620.x |
[81] | Dupuy B, Govind R, Antunes A, et al. (2008) Clostridium difficile toxin synthesis is negatively regulated by TcdC. J Med Microbiol 57: 685-689. doi: 10.1099/jmm.0.47775-0 |
[82] | Tan KS, Wee BY, Song KP (2001) Evidence for holin function of tcdE gene in the pathogenicity of Clostridium difficile. J Med Microbiol 50: 613-619. doi: 10.1099/0022-1317-50-7-613 |
[83] | Mani N, Dupuy B (2001) Regulation of toxin synthesis in Clostridium difficile by an alternative RNA polymerase sigma factor. Proc NatlAcad Sci USA 98: 5844-5849. doi: 10.1073/pnas.101126598 |
[84] | Matamouros S, England P, Dupuy B (2007) Clostridium difficile toxin expression is inhibited by the novel regulator TcdC. Mol Microbiol 64: 1274-1288. doi: 10.1111/j.1365-2958.2007.05739.x |
[85] | Govind R, Dupuy B (2012) Secretion of Clostridium difficile Toxins A and B Requires the Holin-like Protein TcdE. PLoS Pathogens 8: e1002727. doi: 10.1371/journal.ppat.1002727 |
[86] | Eastwood K, Else P, Charlett A, et al. (2009) Comparison of nine commercially available Clostridium difficile toxin detection assays, a real-time PCR assay for C. difficile tcdB, and a glutamate dehydrogenase detection assay to cytotoxin testing and cytotoxigenic culture methods. J Clin Microbiol 47: 3211-3217. |
[87] | Soh YS, Yang JJ, You E, et al. (2014) Comparison of two molecular methods for detecting toxigenic Clostridium difficile. Ann Clin Lab Sci 44: 27-31. |
[88] | Yoo J, Lee H, Park KG, et al. (2015) Evaluation of 3 automated real-time PCR (Xpert C. difficile assay, BD MAX Cdiff, and IMDx C. difficile for Abbott m2000 assay) for detecting Clostridium difficile toxin gene compared to toxigenic culture in stool specimens. Diagn Microbiol Infect Dis 83: 7-10. |
[89] | Lemee L, Dhalluin A, Testelin S, et al. (2004) Multiplex PCR targeting tpi (triose phosphate isomerase), tcdA (toxin A), and tcdB (toxin B) genes for toxigenic culture of Clostridium difficile. J Clin Microbiol 42: 5710-5714. doi: 10.1128/JCM.42.12.5710-5714.2004 |
[90] | Houser BA, Hattel AL, Jayarao BM (2010) Real-time multiplex polymerase chain reaction assay for rapid detection of Clostridium difficile toxin-encoding strains. Foodborne Pathog Dis 7: 719-726. doi: 10.1089/fpd.2009.0483 |
[91] | Rupnik M, Janezic S (2016) An update on Clostridium difficile toxinotyping. J Clin Microbiol 54: 13-18. doi: 10.1128/JCM.02083-15 |
[92] | Bidet P, Barbut F, Lalande V, et al. (1999) Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing. FEMS Microbiol Lett 175: 261-2666. doi: 10.1111/j.1574-6968.1999.tb13629.x |
[93] | Gebreyes WA, Adkins PR (2015) The use of pulsed-field gel electrophoresis for genotyping of Clostridium difficile. Methods Mol Biol 1301: 95-101. doi: 10.1007/978-1-4939-2599-5_9 |
[94] | Killgore G, Thompson A, Johnson S, et al. (2008) Comparison of seven techniques for typing international epidemic strains of Clostridium difficile: restriction endonuclease analysis, pulsed-field gel electrophoresis, PCR-ribotyping, multilocus sequence typing, multilocus variable-number tandem-repeat analysis, amplified fragment length polymorphism, and surface layer protein A gene sequence typing. J Clin Microbiol 46: 431-437. doi: 10.1128/JCM.01484-07 |
[95] | Griffiths D, Fawley W, Kachrimanidou M, et al. (2009) Multilocus sequence typing of Clostridium difficile. J Clin Microbiol 48: 770-778. |
[96] | van den Berg RJ, Schapp I, Templeton KE, et al. (2007) Typing and subtyping of Clostridium difficile isolates using multiple-locus variable-number tandem-repeat analysis. J Clin Microbiol 45: 1024-1028. doi: 10.1128/JCM.02023-06 |