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

Kumar, Anand; Davenport, Karen W.; Vuyisich, Grace; Kunde, Yuliya A.; Johnson, Shannon L.; Chain, Patrick; Dichosa, Armand E. K.; Rodriguez-Palacios, Alexander

doi:10.1128/mra.00853-18

Cited by 13 publications

(20 citation statements)

References 11 publications

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“…To test if the incubation of CD spores in non-reduced media (e.g., agar freshly removed from refrigerator) inhibits CD recovery, we conducted experiments in vitro. Using 1-year-aged spores from human PCR-ribotypes 078, 027, 077, strains 630 and ATCC 1869 (13,28,53), we observed that the use of non-reduced agars results in no CD recovery compared to using agars pre-reduced in an anaerobic chamber 4 h prior inoculation (0/10 vs. 10/10, Fisher exact p < 0.001). Because 26.9% of studies also reported short periods of incubation (e.g., overnight), we determined if short incubation influenced CD recovery.…”

Section: Heterogeneity and Overall Prevalence Of C Difficile In Foodmentioning

confidence: 86%

“…Although earlier articles speculated that the identification of CD in foods could have been due to poor techniques and cross-contamination, high-quality studies have shown that contamination is an obsolete argument to discount the value of identifying toxigenic and even emerging virulent strains of CD in the food supply, which have been shown to be genetically similar to strains of clinical relevance in distant regions (13). Because a number of studies reported 0% of CD, it is possible that there are natural sources of contamination heterogeneity in foods, similarly to other known foodborne pathogens.…”

Section: Discussionmentioning

confidence: 99%

“…With the availability of genomics, elegant studies have shown that only ∼25-30% of CDI in hospitals are nosocomial, redirecting the attention to foods as viable sources of CD (11,12). 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).…”

Section: Introductionmentioning

confidence: 99%

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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

Rodriguez-Palacios

Shah

et al. 2020

Front. Med.

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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 Rodriguez-Palacios et al. Clostridium difficile in Human Diet 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.

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Section: Heterogeneity and Overall Prevalence Of C Difficile In Foodmentioning

confidence: 86%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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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

Rodriguez-Palacios

Shah

et al. 2020

Front. Med.

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show abstract

“…To test if the incubation of CD spores in non-reduced media (e.g., agar freshly removed from refrigerator) inhibits CD recovery, we conducted experiments in vitro. Using 1-year-aged spores from human PCR-ribotypes 078, 027, 077, strains 630 and ATCC 1869 7,36,65 , we observed that the use of non-reduced agars results in no CD recovery compared to using agars pre-reduced in an anaerobic chamber 4 hours prior inoculation (0/10 vs. 10/10, Fisher exact p<0.001). Because 26.9% of studies also reported short periods of incubation (e.g., overnight), we determined if short incubation influenced CD recovery.…”

Section: Heterogeneity and Overall Prevalence Of C Difficile In Foodmentioning

confidence: 86%

“…As historically highlighted, we emphasize that there is molecular evidence that the presence of CD in the human diet is genuine and not due to laboratory cross contamination with CD from human specimens. Major examples include the complete genome sequence of the first food derived PCR-ribotype 078 isolates from foods in Canada that matched contemporary strains affecting humans in the UK, in the mid 2000s, when there was no physical connection between the laboratories that reported both studies 7 . Supporting the remarkable risk for CD exposure via seafoods, we also highlight the latest report of CD in foods conducted in the Adriatic Sea where mussels and clams contaminated at a mean prevalence of 16.9% (CI: 14.1%-19.8%) carried a large proportion of CD representing diverse genotypes commonly isolated in European hospitals (113 CD isolates represented 53 genotypes, with 40.7% of them belonging to CD seen in CDI in hospitals).…”

Section: Discussionmentioning

confidence: 99%

Global and Historical Distribution ofClostridioides difficilein the Human Diet (1981-2019): Systematic Review and Meta-Analysis of 21886 Samples Reveal Sources of Heterogeneity, High-Risk Foods, and Unexpected Higher Prevalence Towards the Tropic

Rodriguez-Palacios

Shah

et al. 2019

Preprint

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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, 21,886 food samples were tested for CD between 1981 and 2019 (232 food-sample-sets; 79 studies; 25 countries). Culture methodology, sample size and type, region, and latitude were significant 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), 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 nonrandom-source of foodborne exposure that occurs independently of laboratory culture methods, across regions, and at variable level depending on food type and latitude. The latitudinal trend (high CD-food-prevalence towards tropic) is inverse to the epidemiological observations of CD-infections (frequent in temperate regions). Findings suggests the plausible hypothesis that ecologically-richer microbiomes in the tropic might protect against intestinal CD colonization/infections despite CD ingestion.

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Fructooligosaccharides and mannose affect Clostridium difficile adhesion and biofilm formation in a concentration-dependent manner

Piotrowski

Wultańska

Obuch-Woszczatyński

et al. 2019

Eur J Clin Microbiol Infect Dis

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The aim of this study was to investigate the effects that prebiotic and candidates for prebiotics on Clostridium difficile strains to adhere to various human epithelial cell lines and to compare the adhesive properties of specific C. difficile strains. We also sought to examine the effect of different concentrations of fructooligosaccharides and mannose on the formation of biofilms by C. difficile strains. The influence of cellobiose, fructooligosaccharides, inulin, mannose, and raffinose on the adherence properties of various C. difficile strains, including motile 630, non-motile M120, and 10 clinical motile ribotype 027 strains, to non-mucous secreting HT-29, mucous secreting HT-29 MXT, and CCD 841 CoN cells lines. The most effective prebiotics were used in biofilm formation assays. We demonstrated that all C. difficile strains adhered to all cell lines. However, the C. difficile M120 non-motile strain was statistically more likely to adhere to all three cell lines (CFU median, 40) compared to the motile strains (CFU median, 3; p < 0.001). Furthermore, among the carbohydrates examined, only fructooligosaccharides and mannose were found to significantly decrease adhesion (p < 0.001) of C. difficile strains. Alternatively, using a biofilm assay, we observed, via confocal laser scanning microscopy, that sub-inhibitory concentrations (1%) of fructooligosaccharides and mannose functioned to increase biofilm formation by C. difficile. We demonstrated that specific prebiotics and candidate prebiotics exhibit varying anti-adhesive properties towards C. difficile in vitro and that treatment with sub-inhibitory concentrations of prebiotics can cause an increase in biofilm formation by C. difficile.

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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

Cited by 13 publications

References 11 publications

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

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

Global and Historical Distribution ofClostridioides difficilein the Human Diet (1981-2019): Systematic Review and Meta-Analysis of 21886 Samples Reveal Sources of Heterogeneity, High-Risk Foods, and Unexpected Higher Prevalence Towards the Tropic

Fructooligosaccharides and mannose affect Clostridium difficile adhesion and biofilm formation in a concentration-dependent manner

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