Global prevalence of Clostridioides difficile in 17,148 food samples from 2009 to 2019: a systematic review and meta-analysis
Journal of Health, Population and Nutrition volume 42, Article number: 36 (2023)
Clostridioides (Clostridium) difficile is an important infectious pathogen, which causes mild-to-severe gastrointestinal infections by creating resistant spores and producing toxins. Spores contaminated foods might be one of the most significant transmission ways of C. difficile-associated infections. This systematic review and meta-analysis study were conducted to investigate the prevalence of C. difficile in food.
Articles that published the prevalence of C. difficile in food in PubMed, Web of Science, and Scopus databases were retrieved using selected keywords between January 2009 and December 2019. Finally, 17,148 food samples from 60 studies from 20 countries were evaluated.
The overall prevalence of C. difficile in various foods was 6.3%. The highest and lowest levels of C. difficile contamination were detected to seafood (10.3%) and side dishes (0.8%), respectively. The prevalence of C. difficile was 4% in cooked food, 6.2% in cooked chicken and 10% in cooked seafood.
There is still little known concerning the food-borne impact of C. difficile, but the reported contamination might pose a public health risk. Therefore, to improve the food safety and prevent contamination with C. difficile spores, it is necessary to observe hygienic issues during foods preparation, cooking and transfer.
In the mid-1970s, the gram-positive and anaerobic bacterium Clostridioides difficile (formerly known as Clostridium difficile) was found as a common cause for nosocomial infection and a major cause of antibiotic-associated diarrhea [1,2,3]. By forming resistant spores and the ability of producing toxins, C. difficile is responsible for a diverse group of infection, from mild and self-limiting gastrointestinal infections to severe life threatening infections, like toxic megacolon [4, 5]. C. difficile infection (CDI) is associated with significant mortality and increased healthcare costs in the world [6,7,8,9]. C. difficile is basically a nosocomial pathogen, but the prevalence of community-acquired CDI seems to be increasing [10, 11]. Prevalence of C. difficile contamination in food is high, and a wide range of foods are contaminated by C. difficile [12, 13]. Therefore, consumption of C. difficile contaminated food is a risk factor for transmission of this infection in community, and one of the most important route of transmitting could be contaminated food by C. difficile spore [14, 15]. The presence of C. difficile in sewage-treatment plants might be a major reason of its community acquisition, transmission to food, and ultimately food contamination [14, 16]. This issue demands more attention to this health-threatening pathogen.
The main aims of this systematic and meta-analysis study were (i) to investigate the prevalence of C. difficile in different types of food and compare them with each other, (ii) to determine the frequency of toxin genes, (iii) to assay the relationship of toxin genes with the prevalence of C. difficile, and (iv) to evaluate the phenotypic and genotypic diagnostic methods from 17,148 food samples.
Published studies from January 2009 to December 2019 were retrieved from four main databases including Web of sciences, Scopus, PubMed, and Google Scholar by applying the following keywords: “clostridia”, “Clostridium spp.”, “Clostridium difficile”, “Clostridioides difficile”, “C. difficile”, “antibiotic resistance”, “food contamination”, “toxinotype”, “ribotype”, and “toxin genes” alone or combined with ‘‘AND’’ and/or ‘‘OR’’ operators. To conduct the present study, Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guideline were considered .
All cross-sectional studies focusing on the prevalence of C. difficile contamination in food samples were included. Short communications, cohort studies, clinical trials, letter to editors, narrative or systematic reviews, and the non-English articles were excluded.
Selection of studies and data gathering
The text of all included studies was accurately read by two independent authors, and in case of any discrepancy, the issue was discussed by other authors to be resolved. The following characteristics of each study were collected: first author, year of publication, sampling year, the location of the study, detection methods, sample type, sample size, the number of detected C. difficile, toxinotypes, ribotypes, toxin genes, antibiotics used, number of resistance isolates, and the method of antibiotic susceptibility assay.
Data analyses were performed using Comprehensive Meta-Analysis software, V2.2.064. The C. difficile prevalence in different food samples and the prevalence of toxinotype and toxin genes, and antibiotic resistance rate in the C. difficile isolates were shown with event rate and a 95% confidence interval (CI). The random-effects model was chosen for meta-analyses, and several subgroup analyses were conducted to evaluate the source of heterogeneity based on the continent, country, sample types and the sampling periods of time. Using a random-effects model, risk ratios for each sample type were calculated to quantify the differences and rank the sample types based on the risk. The Q test and I2 statistic were applied to measure any possible heterogeneity between the studies. The publication bias was evaluated by conducting Egger weighted regression test. In all analyses, the significate threshold was < 0.05 (p value < 0.05).
In total, 2202 studies were recovered after accurate searching in the databases using the aforementioned key words. Among them, 1026 papers were non-duplicated articles and were considered in the study. After title/abstract screening, 116 studies remained. For eligibility, 79 studies were assessed by full-text reading. Sixty studies remained for final qualitative and meta-analysis. The diagram of our search strategy is given in Fig. 1, and the extracted characteristics of the studies are shown in Table 1.
The pooled prevalence of C. difficile in food samples
To analyze the pooled prevalence of C. difficile in food samples, 60 studies were used in a random-effects model. The event rate, which was the number of C. difficile cases over the number of samples, was applied as the effect size index. The overall pooled prevalence of C. difficile in food samples was estimated to be 6.3% (CI 95%: 4.8–8.2) (Fig. 2). The lowest and highest C. difficile prevalence was observed in Shaughnessy et al. and Romano et al. reports with 0.1% and 66.7% prevalence, respectively (Fig. 2). The Q-value was 1049.1 which was much higher than the number of studies minus 1 (60–1 = 59), that reject the null hypothesis and showed a significant heterogeneity between studies. The I2 statistics indicated that 94.4% of the variances reflect true variances between studies.
Subgroup analysis of C. difficile prevalence based on the study continent, the year of sampling and the sample types
To subgroup analysis of C. difficile prevalence in food samples was performed based on the study continent, in which the 60 studies were divided into the following subgroups: Africa (two studies), Asia (20 studies), Central/North America (20 studies), Europe (17 studies), and South America (one study). Difference in prevalence of C. difficile isolated from food samples in different continents was not significant (Table 2).
To subgroup analysis of C. difficile food prevalence based on the sampling year, three time frames were used as follows: TF1 (2004-the end of 2008), TF2 (2009-the end of 2013), and TF3 (2014 ≤). Considering these time frames, 44 studies were used for a random-effects model subgroup analysis. No statistically significant difference was observed between time frame subgroups (Table 2).
To subgroup analysis of C. difficile food prevalence based on the sample type, the following subgroups were used: raw meat (R-meat), cooked meat/Hamburger (C-meat/Ham), poultry raw meat (R-poultry), cooked poultry (C-poultry), raw seafood/fish (Seafood), cooked seafood/fish (C-seafood), vegetables (Veg.), ready-to-eat meat (RTE meat), Milk/Dairy, salad, soy, side dishes (S-dishes), and pet food. The prevalence of C. difficile in each sample type is presented in Table 2. The highest and lowest prevalence were 10.3% and 0.8%, which were seen in Seafood and S-dishes sample types, respectively (Table 2). Although there were some differences in C. difficile prevalence of different sample types, no significant heterogeneity was observed between groups (Q-value: 10.657, p value: 0.557) (Table 2).
For better presentation of the results, in another arrangement, the studies were divided to more general groups based on sample types as follows: meat, poultry, seafood, vegetables, salad, milk/diary, and others (S-dishes, soy, pet food) (Fig. 3).
For presenting each sample type in each country, more subgroup analyses were performed. The summary results of these analyses are shown in Fig. 4. Also, risk ratios were obtained using the extracted data. Based on the ranking of the risk ratio, S-dishes as a reference and was the lowest source of C. difficile and seafood, RTE meat, C-poultry, salad, R-poultry and R-meat had highest risks. Compared to S-dishes, the probability of contamination of seafood with CD was 12.88 times higher than S-dishes, and the risk of contamination of RTE meat, C-poultry, salad, R-poultry and R-meat obtained 9.75, 7.75, 7.63, 7.63 and 7.0 times more than S-dishes, respectively (Fig. 5).
Prevalence of C. difficile ribotype, toxinotypes and toxin genes
According to a very diverse reported ribotypes, it was impossible to analyze the pooled prevalence of the ribotypes; this parameter is represented in Additional file 1: Table S1 without further analysis.
The most frequent toxinotypes of C. difficile were toxinotype 0, III, and V. As it is shown in Table 3, the toxinotype V was more prevalent comparing to other two toxinotypes, and there was a significant heterogeneity between the toxinotypes (Q-value: 9.725, p value: 0.008) (Table 3).
The toxin genes that were reported in more than one study include genes A, B, CTD, tcdC, tcdC18, tcdC39, tcdC117, and cdtA. The toxin genes of A and B were the most frequent, and genes tcdC18 and tcdC117 were the lowest frequent genes studied (Table 3). There was also significant heterogeneity between the studied genes (Q-value: 58.9, p value: 0.000) (Table 3).
As shown in Table 4, toxin type 0 in which pathogenic strains were located shows a higher prevalence in seafood samples. While the prevalence of toxin types 3 and 5 was higher in RTE meat and R-poultry. As shown in Table 5, the highest prevalence of toxin genes A, B, and CDT was observed in RTE meat samples. Compared to other samples, Milk/Dairy and Salad rank after RTE meat in terms of the high prevalence of genes A and B toxins.’
The publication bias was checked based on the pooled prevalence of C. difficile isolates in food samples. The Egger’s linear regression test result showed a significant publication bias in the included studies (p value < 0.0001).
Consuming the contaminated raw and cooked foods with C. difficile spore might be an important route of its transmission [18,19,20]. Food contamination has played an important role in epidemiology of some infectious diseases, but little information is available about the global frequency of C. difficile in food products [21, 22]. The present study analyzed the distribution of C. difficile in 60 studies published from 2009 to 2019 in 17,148 food samples. The results showed that the overall prevalence of C. difficile in all food samples was 6.3%, with the lowest and highest prevalence of C. difficile were 0.1% and 66.7%, respectively. In a systematic review study, Rodriguez-Palacios and colleagues reported the 4.1% prevalence of C. difficile in human diet samples during 1981 to 2018 . Comparing to the results presented in this study, it seems that the reported prevalence of the bacterium in these two studies is quiet the same. Taken together, the overall C. difficile prevalence in food samples in the world seems to be less than 10%, but it is relatively high and should not be undermined.
Significant heterogeneity was observed between the studies that indicated different prevalence of C. difficile in different parts of the world. However, in addition to real differences in C. difficile prevalence, the observed heterogeneity may be due to different seasons of sampling, temperatures and geographical conditions, the quality of studies, the sensitivity of detection methods, etc. . Although the frequency of C. difficile varied in food samples from different continents, these differences were not statistically significant. The prevalence of C. difficile in Asia and Europe was almost the same, but it was lower in Africa and North/Central America comparing to similar reports . In this study, this difference could be attributed to high consumption of seafood’s in diet of Asia and Europe, and a large number of seafood samples have been studied. The lowest prevalence of C. difficile was observed in South America.
Most of the studies were on meat and meat products. The contamination of undercooked and prepared foods was evident . The prevalence of C. difficile in meat products of this study was the same as a report by Usui 2020 , but was lower than study reported from Canada by Warriner in 2017 . It must be noted that the prevalence of food sample isolated C. difficile was so variable with a range of 1.6% from Netherlands  to 42% from USA . The prevalence of C. difficile in chicken and poultry meat was 6.2%, which was similar to the previous study (6.7%) . However, the isolation rate of C. difficile from chicken meat samples was ranging from %0 [29,30,31] to 44.4% in turkey meat samples . It seems that the chicken with skin is more vulnerable to contamination comparing to skin-less chicken samples .
Seafood and oysters well-known carriers of C. difficile . In the present meta-analysis, the overall contamination rate of seafood was 10.3% and had the highest risk ratio (12.88%). According to another meta-analysis study, pooled prevalence of C. difficile in seafood was shown a little bit more in comparison with our pooled prevalence (Seafood risk ratio was 14.3) . This difference may be because of longer time and more included studies. The variation between prevalence of C. difficile isolated from seafood’s have been seen in many studies from around the world ranged from 3.9% to more than 40% [35,36,37]. The first report of root vegetables contamination with C. difficile was in 1996 .
In this study, the overall prevalence of C. difficile in contaminated vegetables was 5.7%, which was less than another meta-analysis (12% on average). This would be due to the increase of health level in production and transfer of vegetables [25, 26].
Regardless of the type of food products, the most important issue in relation to C. difficile strains is detecting their ribotypes and toxinotypes . Although we could not statistically analyze the C. difficile ribotypes data due to vast divergence of the informations, it is obvious that ribotypes 027 and 078 were the most predominants followed by 001 [20, 39], 010  and 020/014  ribotypes. The results of the present study showed that the most common toxinotypes were toxinotypes were toxinotype V, 0, III, respectively. In a review study, the presence of toxin genes in food samples was estimated as 3.5%  to 100% [31, 32, 37]. The types of toxinotypes can be important in the development of molecular diagnostic tests and vaccines .
As reported by many studies C. difficile harboring tcdA and tcdB, toxin genes were more prevalent than other strains .
The contamination risk analysis showed that seafood and RTE-meat are the high-risk foods. While in Rodriguez-Palacios study (21), among different food items, vegetables and seafood were ranked as the high-risk food items, in both studies, seafood is one of the risk food items. This information can be useful for determining preventive food safety measures (cooking food and not consuming raw food) to minimize the possibility of further food contamination.
This study showed that a variety of foods, especially seafood, were at potential risk for C. difficile. The frequency of C. difficile varied in food samples from different continents. This difference can be attributed to the high consumption of seafood in the diet of Asia and Europe. These results suggest that consumption of raw and undercooked foods is a way to further transmit C. difficile to humans.
Therefore, enough cooking of food, suitable washing of animal carcasses in the slaughter process, prevention of carcass contamination with animal feces play an important role in increasing food safety.
Availability of data and materials
All relevant data are within the manuscript and its Supporting Information files.
Moono P, Foster NF, Hampson DJ, Knight DR, Bloomfield LE, Riley TV. Clostridium difficile infection in production animals and avian species: a review. Foodborne Pathog Dis. 2016;13(12):647–55.
Freeman J, Bauer M, Baines SD, Corver J, Fawley W, Goorhuis B, et al. The changing epidemiology of Clostridium difficile infections. Clin Microbiol Rev. 2010;23(3):529–49.
Dinleyici M, Vandenplas Y. Clostridium difficile colitis prevention and treatment. Adv Exp Med Biol. 2019;1125:139–46.
Bartlett JG, Chang TW, Gurwith M, Gorbach SL, Onderdonk AB. Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. N Engl J Med. 1978;298(10):531–4.
Lawson PA, Citron DM, Tyrrell KL, Finegold SM. Reclassification of clostridium difficile as Clostridioides difficile (Hall and O’Toole 1935) Prévot 1938. Anaerobe. 2016;40:95–9.
Leffler DA, Lamont JT. Clostridium difficile infection. N Engl J Med. 2015;372(16):1539–48.
Brown KA, Fisman DN, Moineddin R, Daneman N. The magnitude and duration of Clostridium difficile infection risk associated with antibiotic therapy: a hospital cohort study. PLoS ONE. 2014;9(8): e105454.
Gutiérrez-Pizarraya A, Martín-Villén L, Alcalá-Hernández L, Arriaza MM, Balandín-Moreno B, Aragón-González C, et al. Epidemiology and risk factors for Clostridium difficile infection in critically ill patients in Spain: the PROCRID study. Enferm Infecc Microbiol Clin (Engl Ed). 2018;36(4):218–21.
Habayeb H, Sajin B, Patel K, Grundy C, Al-Dujaili A, Van de Velde S. Amoxicillin plus temocillin as an alternative empiric therapy for the treatment of severe hospital-acquired pneumonia: results from a retrospective audit. Eur J Clin Microbiol Infect Dis. 2015;34(8):1693–9.
Guh AY, Mu Y, Winston LG, Johnston H, Olson D, Farley MM, et al. Trends in US burden of Clostridioides difficile infection and outcomes. N Engl J Med. 2020;382(14):1320–30.
Kumar GV, Uma B. Clostridium difficile: a neglected, but emerging pathogen in India. Arch Clin Microbiol. 2015;6(2):1–5.
Gould LH, Limbago B. Clostridium difficile in food and domestic animals: a new foodborne pathogen? Clin Infect Dis. 2010;51(5):577–82.
Candel-Pérez C, Ros-Berruezo G, Martínez-Graciá C. A review of Clostridioides [Clostridium] difficile occurrence through the food chain. Food Microbiol. 2019;77:118–29.
Rodriguez C, Taminiau B, Broeck JV, Delmée M, Daube G. Clostridium difficile in food and animals: a comprehensive review. Adv Exp Med Biol. 2016;932:65–92.
Knetsch C, Connor TR, Mutreja A, Van Dorp S, Sanders I, Browne H, et al. Whole genome sequencing reveals potential spread of Clostridium difficile between humans and farm animals in the Netherlands, 2002 to 2011. Euro Surveill. 2014;19(45):20954.
Knetsch C, Kumar N, Forster S, Connor T, Browne H, Harmanus C, et al. Zoonotic transfer of Clostridium difficile harboring antimicrobial resistance between farm animals and humans. J Clin Microbiol. 2018;56(3):e01384-e1417.
McInnes MD, Moher D, Thombs BD, McGrath TA, Bossuyt PM, Clifford T, et al. Preferred reporting items for a systematic review and meta-analysis of diagnostic test accuracy studies: the PRISMA-DTA statement. JAMA. 2018;319(4):388–96.
Broda DM, Delacy KM, Bell RG, Braggins TJ, Cook RL. Psychrotrophic Clostridium spp. associated with ‘blown pack’spoilage of chilled vacuum-packed red meats and dog rolls in gas-impermeable plastic casings. Int J Food Microbiol. 1996;29(2–3):335–52.
Borriello S, Honour P, Turner T, Barclay F. Household pets as a potential reservoir for Clostridium difficile infection. J Clin Pathol. 1983;36(1):84–7.
Tkalec V, Janezic S, Skok B, Simonic T, Mesaric S, Vrabic T, et al. High Clostridium difficile contamination rates of domestic and imported potatoes compared to some other vegetables in Slovenia. Food Microbiol. 2019;78:194–200.
Rodriguez-Palacios A, Mo KQ, Shah BU, Msuya J, Bijedic N, Deshpande A, et al. Global and historical distribution 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 prevalence toward the tropic. Front Med (Lausanne). 2020;7:9.
Kumar A, Davenport KW, Vuyisich G, Kunde YA, Johnson SL, Chain PSG, et al. Complete genome sequences of historic Clostridioides difficile food-dwelling ribotype 078 strains in Canada identical to that of the historic human clinical strain M120 in the United Kingdom. Microbiol Resour Announc. 2018;7(12):e00853-e918.
Guernier V, Hochberg ME, Guégan J-F. Ecology drives the worldwide distribution of human diseases. PLoS Biol. 2004;2(6): e141.
Rodriguez C, Avesani V, Van Broeck J, Taminiau B, Delmée M, Daube G. Presence of Clostridium difficile in pigs and cattle intestinal contents and carcass contamination at the slaughterhouse in Belgium. Int J Food Microbiol. 2013;166(2):256–62.
Usui M, Maruko A, Harada M, Kawabata F, Sudo T, Noto S, et al. Prevalence and characterization of Clostridioides difficile isolates from retail food products (vegetables and meats) in Japan. Anaerobe. 2020;61: 102132.
Warriner K, Xu C, Habash M, Sultan S, Weese S. Dissemination of Clostridium difficile in food and the environment: significant sources of C. difficile community-acquired infection? J Appl Microbiol. 2017;122(3):542–53.
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(3):561–4.
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(5):819–21.
Ersöz ŞŞ, Coşansu S. Prevalence of Clostridium difficile isolated from beef and chicken meat products in Turkey. Korean J Food Sci Anim Resour. 2018;38(4):759–67.
Indra A, Lassnig H, Baliko N, Much P, Fiedler A, Huhulescu S, et al. Clostridium difficile: a new zoonotic agent? Wien Klin Wochenschr. 2009;121(3–4):91–5.
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(8):1732–4.
Hasannejad-Bibalan M, Avarvand AY, Malekzadegan Y, Sabati H, Amini ME, Ebrahim-Saraie HS. Prevalence of Clostridium difficile contamination in Iranian foods and animals: a systematic review and meta-analysis. Gene Rep. 2020;21: 100898.
Heise J, Witt P, Maneck C, Wichmann-Schauer H, Maurischat S. Prevalence and phylogenetic relationship of Clostridioides difficile strains in fresh poultry meat samples processed in different cutting plants. Int J Food Microbiol. 2021;339: 109032.
Romano V, Pasquale V, Krovacek K, Mauri F, Demarta A, Dumontet S. Toxigenic Clostridium difficile PCR ribotypes from wastewater treatment plants in southern Switzerland. Appl Environ Microbiol. 2012;78(18):6643–6.
Troiano T, Harmanus C, Sanders IM, Pasquale V, Dumontet S, Capuano F, et al. Toxigenic Clostridium difficile PCR ribotypes in edible marine bivalve molluscs in Italy. Int J Food Microbiol. 2015;208:30–4.
Pasquale V, Romano V, Rupnik M, Capuano F, Bove D, Aliberti F, et al. Occurrence of toxigenic Clostridium difficile in edible bivalve molluscs. Food Microbiol. 2012;31(2):309–12.
Montazeri N, Liu D, Janes ME. Occurrence of toxigenic Clostridium difficile in Louisiana Oysters (Crassostrea virginica) and environmental waters. J Food Nutr Sci. 2015;6(11):1065–70.
Al Saif N, Brazier J. The distribution of Clostridium difficile in the environment of South Wales. J Med Microbiol. 1996;45(2):133–7.
Koene M, Mevius D, Wagenaar J, Harmanus C, Hensgens M, Meetsma A, et al. Clostridium difficile in Dutch animals: their presence, characteristics and similarities with human isolates. Clin Microbiol Infect. 2012;18(8):778–84.
Rupnik M, Janezic S. An update on Clostridium difficile toxinotyping. J Clin Microbiol. 2016;54(1):13–8.
Abdel-Glil MY, Thomas P, Schmoock G, Abou-El-Azm K, Wieler LH, Neubauer H, et al. Presence of Clostridium difficile in poultry and poultry meat in Egypt. Anaerobe. 2018;51:21–5.
Kouassi KA, Dadie AT, N’Guessan KF, Dje KM, Loukou YG. Clostridium perfringens and Clostridium difficile in cooked beef sold in Cote d’Ivoire and their antimicrobial susceptibility. Anaerobe. 2014;28:90–4.
Esfandiari Z, Weese S, Ezzatpanah H, Jalali M, Chamani M. Occurrence of Clostridium difficile in seasoned hamburgers and seven processing plants in Iran. BMC Microbiol. 2014;14:283.
Esfandiari Z, Jalali M, Ezzatpanah H, Weese JS, Chamani M. Prevalence and characterization of Clostridium difficile in beef and mutton meats of Isfahan region, Iran. Jundishapur J Microbiol. 2014;7(8): e16771.
Esfandiari Z, Jalali M, Ezzatpanah H, Weese JS, Chamani M. The Frequency of Clostridium difficile in processing steps of hamburger. HSR. 2013;9(13):1460–8.
Esfandiari Z, Jalali M, Ezzatpanah H, Weese S, Chamani M. Examination of Clostridium difficile Contamination in beef meat distributed in Isfahan using culture and Multiplex-PCR method. BJM. 2014;3(11):109–16.
Hasanzade A, Rahimi E. Isolation of Clostridium difficile from Turkey and ostrich meat sold in meat stores if Isfahan city. Int J Adv Biol Biomed Res. 2013;1(9):963–7.
Hasanzadeh A, Rahimi E. Isolation of Clostridium difficile from chicken meat sold in meat stores of Isfahan City. Adv Environ Biol. 2013;7(9):2372–4.
Kheradmand M, Jalilian S, Alvandi A, Abiri R. Prevalence of Clostridium difficile and its toxigenic genotype in beef samples in west of Iran. Iran J Microbiol. 2017;9(3):169–73.
Knight DR, Putsathit P, Elliott B, Riley TV. Contamination of Australian newborn calf carcasses at slaughter with Clostridium difficile. Clin Microbiol Infect. 2016;22(3):266.e1-7.
Kochakkhani H, Moosavy MH, Dehghan P. Isolation and identification of Clostridium difficile from ready-to-eat vegetable salads in restaurants of Tabriz by Real-time PCR and determination of the antibiotic resistance pattern. SJKUMS. 2017;22(3):102–12.
Lee JY, Lee DY, Cho YS. Prevalence of Clostridium difficile isolated from various raw meats in Korea. Food Sci Biotechnol. 2018;27(3):883–9.
Lim S, Foster N, Elliott B, Riley T. High prevalence of Clostridium difficile on retail root vegetables, Western Australia. J Appl Microbiol. 2018;124(2):585–5890.
Nayebpour F, Rahimi E. Retracted: prevalence, antibiotic resistance, and toxigenic gene profile of the Clostridium difficile isolated from molluscan shellfish. J Food Saf. 2019;39(1): e12586.
Rahimi E, Jalali M, Weese JS. Prevalence of Clostridium difficilein raw beef, cow, sheep, goat, camel and buffalo meat in Iran. BMC Public Health. 2014;14:119.
Rahimi E, Afzali ZS, Baghbadorani ZT. Clostridium difficile in ready-to-eat foods in Isfahan and Shahrekord. Iran Asian Pac J Trop Biomed. 2015;5(2):128–31.
Rahimi E, Khaksar F. Detection of toxigenic Clostridium difficile strains isolated from meat and meat products in Iran. B J Vet Med. 2015;18(3):277–81.
Razmyar J, Jamshidi A, Khanzadi S, Kalidari G. Toxigenic Clostridium difficile in retail packed chicken meat and broiler flocks in northeastern Iran. Iran J Vet Res. 2017;18(4):271–4.
Rivas L, Dupont PY, Gilpin B, Cornelius A. Isolation and characterization of Clostridium difficile from a small survey of wastewater, food and animals in New Zealand. Lett Appl Microbiol. 2020;70(1):29–35.
Wu Y-C, Chen C-M, Kuo C-J, Lee J-J, Chen P-C, Chang Y-C, et al. Prevalence and molecular characterization of Clostridium difficile isolates from a pig slaughterhouse, pork, and humans in Taiwan. Int J Food Microbiol. 2017;242:37–44.
Yamoudy M, Mirlohi M, Isfahani BN, Jalali M, Esfandiari Z, Hosseini NS. Isolation of toxigenic Clostridium difficile from ready-to-eat salads by multiplex polymerase chain reaction in Isfahan, Iran. Adv Biomed Res. 2015;4:87.
Zamani AH, Razmyar J, Berger FK, Kalidari GA, Jamshidi A. Isolation and toxin gene detection of Clostridium (Clostridioides) difficile from traditional and commercial quail farms and packed quail meat for market supply–short communication. Acta Vet Hung. 2019;67(4):499–504.
Curry SR, Marsh JW, Schlackman JL, Harrison LH. Prevalence of Clostridium difficile in uncooked ground meat products from Pittsburgh, Pennsylvania. Appl Environ Microbiol. 2012;78(12):4183–6.
Quesada-Gómez C, Mulvey MR, Vargas P, del Mar G-C, Rodríguez C, Rodríguez-Cavillini E. Isolation of a toxigenic and clinical genotype of Clostridium difficile in retail meats in Costa Rica. J Food Prot. 2013;76(2):348–51.
Han Y, King J, Janes ME. Detection of antibiotic resistance toxigenic Clostridium difficile in processed retail lettuce. Food Qual Saf. 2018;2(1):37–41.
Harvey RB, Norman KN, Andrews K, Norby B, Hume ME, Scanlan CM, et al. Clostridium difficile in retail meat and processing plants in Texas. J Vet Diagn Invest. 2011;23(4):807–11.
Harvey RB, Norman KN, Andrews K, Hume ME, Scanlan CM, Callaway TR, et al. Clostridium difficile in poultry and poultry meat. Foodborne Pathog Dis. 2011;8(12):1321–3.
Hawken P, Weese JS, Friendship R, Warriner K. Carriage and dissemination of Clostridium difficile and methicillin resistant Staphylococcus aureus in pork processing. Food Control. 2013;31(2):433–7.
Hawken P, Weese JS, Friendship R, Warriner K. Longitudinal study of Clostridium difficile and Methicillin-resistant Staphylococcus aureus associated with pigs from weaning through to the end of processing. J Food Prot. 2013;76(4):624–30.
Houser BA, Hattel AL, Jayarao BM. Real-time multiplex polymerase chain reaction assay for rapid detection of Clostridium difficile toxin-encoding strains. Foodborne Pathog Dis. 2010;7(6):719–26.
Kalchayanand N, Arthur TM, Bosilevac JM, Brichta-Harhay DM, Shackelford SD, Wells JE, et al. Isolation and characterization of Clostridium difficile associated with beef cattle and commercially produced ground beef. J Food Prot. 2013;76(2):256–64.
Kwon JH, Lanzas C, Reske KA, Hink T, Seiler SM, Bommarito KM, et al. An evaluation of food as a potential source for Clostridium difficile acquisition in hospitalized patients. Infect Control Hosp Epidemiol. 2016;37(12):1401–7.
Metcalf D, Reid-Smith RJ, Avery BP, Weese JS. Prevalence of Clostridium difficile in retail pork. Can Vet J. 2010;51(8):873–6.
Metcalf D, Avery BP, Janecko N, Matic N, Reid-Smith R, Weese JS. Clostridium difficile in seafood and fish. Anaerobe. 2011;17(2):85–6.
Mooyottu S, Flock G, Kollanoor-Johny A, Upadhyaya I, Jayarao B, Venkitanarayanan K. Characterization of a multidrug resistant C. difficile meat isolate. Int J Food Microbiol. 2015;192:111–6.
Norman KN, Harvey RB, Andrews K, Hume ME, Callaway TR, Anderson RC, et al. Survey of Clostridium difficile in retail seafood in College Station, Texas. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2014;31(6):1127–9.
Shaughnessy MK, Snider T, Sepulveda R, Boxrud D, Cebelinski E, Jawahir S, et al. Prevalence and molecular characteristics of Clostridium difficile in retail meats, food-producing and companion animals, and humans in Minnesota. J Food Prot. 2018;81(10):1635–42.
Varshney JB, Very KJ, Williams JL, Hegarty JP, Stewart DB, Lumadue J, et al. Characterization of Clostridium difficile isolates from human fecal samples and retail meat from Pennsylvania. Foodborne Pathog Dis. 2014;11(10):822–9.
Visser M, Sepehrim S, Olson N, Du T, Mulvey MR, Alfa MJ. Detection of Clostridium difficile in retail ground meat products in Manitoba. Can J Infect Dis Med Microbiol. 2012;23(4):244.
Weese JS, Avery BP, Rousseau J, Reid-Smith RJ. Detection and enumeration of Clostridium difficile spores in retail beef and pork. Appl Environ Microbiol. 2009;75(15):5009–11.
Weese J, Reid-Smith R, Avery B, Rousseau J. Detection and characterization of Clostridium difficile in retail chicken. Lett Appl Microbiol. 2010;50(4):362–5.
Agnoletti F, Arcangeli G, Barbanti F, Barco L, Brunetta R, Cocchi M, et al. Survey, characterization and antimicrobial susceptibility of Clostridium difficile from marine bivalve shellfish of North Adriatic Sea. Int J Food Microbiol. 2019;298:74–80.
Bakri MM, Brown DJ, Butcher JP, Sutherland AD. Clostridium difficile in ready-to-eat salads, Scotland. Emerg Infect Dis. 2009;15(5):817–8.
Eckert C, Burghoffer B, Barbut F. Contamination of ready-to-eat raw vegetables with Clostridium difficile in France. J Med Microbiol. 2013;62(9):1435–8.
Guran HS, Ilhak OI. Clostridium difficile in retail chicken meat parts and liver in the Eastern Region of Turkey. J Verbraucherschut Lebensm. 2015;10(4):359–64.
Hampikyan H, Bingol EB, Muratoglu K, Akkaya E, Cetin O, Colak H. The prevalence of Clostridium difficile in cattle and sheep carcasses and the antibiotic susceptibility of isolates. Meat Sci. 2018;139:120–4.
Jöbstl M, Heuberger S, Indra A, Nepf R, Köfer J, Wagner M. Clostridium difficile in raw products of animal origin. I Int J Food Microbiol. 2010;138(1–2):172–5.
Primavilla S, Farneti S, Petruzzelli A, Drigo I, Scuota S. Contamination of hospital food with Clostridium difficile in Central Italy. Anaerobe. 2019;55:8–10.
Rodriguez C, Taminiau B, Avesani V, Van Broeck J, Delmée M, Daube G. Multilocus sequence typing analysis and antibiotic resistance of Clostridium difficile strains isolated from retail meat and humans in Belgium. Food Microbiol. 2014;42:166–71.
Rodriguez C, Korsak N, Taminiau B, Avesani V, Van Broeck J, Brach P, et al. Clostridium difficile from food and surface samples in a Belgian nursing home: an unlikely source of contamination. Anaerobe. 2015;32:87–9.
Romano V, Pasquale V, Lemee L, El Meouche I, Pestel-Caron M, Capuano F, et al. Clostridioides difficile in the environment, food, animals and humans in southern Italy: occurrence and genetic relatedness. Comp Immunol Microbiol Infect Dis. 2018;59:41–6.
Pires RN, Caurio CF, Saldanha GZ, Martins AF, Pasqualotto AC. Clostridium difficile contamination in retail meat products in Brazil. Braz J Infect Dis. 2018;22(4):345–6.
The authors of this article express their gratitude and appreciation to the Vice Chancellor for Research and Technology of Kermanshah University of Medical Science for accepting the costs of implementing this project. The present article has been registered with grand number.
This research was financially supported by Vice-Chancellor for Research and Technology of Kermanshah University of Medical Sciences.
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The study was approved by ethic committee of Kermanshah University of Medical Sciences (ethic number: IR.KUMS.REC.1398.017). Consent to participate, not applicable.
The authors have declared that no competing interests exist.
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Borji, S., Kadivarian, S., Dashtbin, S. et al. Global prevalence of Clostridioides difficile in 17,148 food samples from 2009 to 2019: a systematic review and meta-analysis. J Health Popul Nutr 42, 36 (2023). https://doi.org/10.1186/s41043-023-00369-3