- Open Access
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.
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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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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
- Clostridioides (Clostridium) difficile
- Public health