Abstract
Clostridioides difficile (CD) is a spore-forming bacterium that causes life-threatening intestinal infections in humans. Although formerly regarded as exclusively nosocomial, there is increasing genomic evidence that person-to-person transmission accounts for only <25% of cases, supporting the culture-based hypothesis that foods may be routine sources of CD-spore ingestion in humans. To synthesize the evidence on the risk of CD exposure via foods, we conducted a systematic review and meta-analysis of studies reporting the culture prevalence of CD in foods between January 1981 and November 2019. Meta-analyses, risk-ratio estimates, and meta-regression were used to estimate weighed-prevalence across studies and food types to identify laboratory and geographical sources of heterogeneity. In total, 21886 food samples were tested for CD between 1981 and 2019 (96.4%, n = 21084, 2007–2019; 232 food-sample-sets; 79 studies; 25 countries). Culture methodology, sample size and type, region, and latitude were sources of heterogeneity (p < 0.05). Although non-strictly-anaerobic methods were reported in some studies, and we confirmed experimentally that improper anaerobiosis of media/sample-handling affects CD recovery in agar (Fisher, p < 0.01), most studies (>72%) employed the same (one-of-six) culture strategy. Because the prevalence was also meta-analytically similar across six culture strategies reported, all studies were integrated using three meta-analytical methods. At the study level (n = 79), the four-decade global cumulative-prevalence of CD in the human diet was 4.1% (95%CI = −3.71, 11.91). At the food-set level (n = 232, mean 12.9 g/sample, similar across regions p > 0.2; 95%CI = 9.7–16.2), the weighted prevalence ranged between 4.5% (95%CI = 3–6%; all studies) and 8% (95%CI = 7–8%; only CD-positive-studies). Risk-ratio ranking and meta-regression showed that milk was the least likely source of CD, while seafood, leafy green vegetables, pork, and poultry carried higher risks (p < 0.05). Across regions, the risk of CD in foods for foodborne exposure reproducibly decreased with Earth latitude (p < 0.001). In conclusion, CD in the human diet is a global non-random-source of foodborne exposure that occurs independently of laboratory culture methods, across regions, and at a variable level depending on food type and latitude. The latitudinal trend (high CD-food-prevalence toward tropic) is unexpectedly inverse to the epidemiological observations of CD-infections in humans (frequent in temperate regions). Findings suggest the plausible hypothesis that ecologically-richer microbiomes in the tropic might protect against intestinal CD colonization/infections despite CD ingestion.
Highlights
Clostridioides (Clostridium) difficile (CD) is a spore-forming anaerobic bacterium that causes severe enteritis, colitis, and mortality in susceptible humans, especially if affected with inflammatory bowel diseases, cancer, immunosuppression, or if taking antibiotics [1,2,3,4,5]
The cumulative prevalence of CD in the foods tested has been 4.1% globally at the study-level, we demonstrate that the cumulative prevalence has distinct patterns of heterogeneity depending on the region, being comparably lower at the study-level in Europe (1.9%; 95%CI = −7.49, 11.29; see Figure 5 for cumulative estimates in other regions)
This study encompasses almost 40 years of available reports, which could be perceived as a representation of a wide array of non-comparable culture methodologies, our analysis illustrates that the majority of studies were published over the past 12 years as shown in Table 1 (92.4%, 73 of 79 studies since 2007)
Summary
Clostridioides (Clostridium) difficile (CD) is a spore-forming anaerobic bacterium that causes severe enteritis, colitis, and mortality in susceptible humans, especially if affected with inflammatory bowel diseases, cancer, immunosuppression, or if taking antibiotics [1,2,3,4,5]. To date, it is well-known that CD infections (CDI) in humans are more frequent in temperate regions. As further evidence for connectivity between foods and CDI, last year a de novo genome sequencing study showed that the first CD strain derived from foods (PCR ribotype 078) in Canada in 2005 was identical to the historical strain M120 that contributed to epidemics in the UK in 2007 [13]
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