High Prevalence of Clostridium difficile in Home Gardens in Western Australia

Abstract

In recent years, community-acquired Clostridium difficile infection (CA-CDI) has emerged as a significant health problem, accounting for ∼50% of all CDI cases. We hypothesised that the home garden environment could contribute to the dissemination of C. difficile spores in the community and investigated 23 homes in 22 suburbs of Perth, Western Australia. We identified a high prevalence of toxigenic C. difficile in this environment. In total, 97 samples consisting of soil (n=48), compost (n=15), manure (n=12) and shoe sole swabs (n= 22) were collected. All samples were cultured anaerobically on C. difficile ChromID agar and enriched in brain heart infusion broth, and isolates were characterised by toxin gene PCR and PCR ribotyping. Two-thirds (67%, 95% confidence interval [CI] 57-76%) of home garden samples including 79% (95% CI 68-91%) of soil, 67% (95% CI 43-90%) of compost, 83% (95% CI 62%-100%) of manure and 32% (95% CI 12-51%) of shoe sole samples contained C. difficile. Of 87 isolates, 38% (95% CI 28-48%) were toxigenic, and 26 PCR ribotypes (RTs), five of which were novel, were identified. The toxigenic C. difficile strain RT014/020 was the most prevalent RT. Interestingly, 19 esculin hydrolysis negative strains giving white colonies were identified on C. difficile ChromID agar, five of which were novel toxigenic RTs that produced only toxin A. Clearly, there is the potential for transmission of C. difficile in the community due to the contamination of home gardens. Our findings highlight the importance of a “One Health” approach to dealing with CDI. IMPORTANCE Recently, community-associated Clostridium difficile infection (CA-CDI) has emerged as a significant problem, accounting for ∼50% of all CDI cases and reported to affect a younger population without traditional risk factors. Possible sources of CA-CDI are soil, food and water contaminated by animal faeces, and recent reports show overlapping ribotypes of C. difficile in animals, humans and the environment, however, the epidemiology of CA-CDI and related risk factors need to be better understood. Our research aimed to determine the prevalence of C. difficile in home gardens and on the shoe soles of homeowners in Perth, Western Australia. There were high rates of contamination with C. difficile in gardens, and some of the ribotypes identified had been isolated from human cases of CDI in Western Australia. This study shows that home gardens and shoes may be a source of C. difficile in CA-CDI.

Whole-genome sequencing links Clostridium (Clostridioides) difficile in a single hospital to diverse environmental sources in the community

“…Despite being non-toxigenic (and therefore incapable of causing disease), we decided to sequence RT 010 given its ubiquity to show that it is feasible for C. difficile in the community to be imported into a hospital. In Australia, 35%-65% of the C. difficile isolated from our environmental samples were non-toxigenic (Lim et al, 2018(Lim et al, , 2020Moono et al, 2017;Perumalsamy et al, 2019;Shivaperumal et al, 2020) and similar observations were made in Europe (Janezic et al, 2016(Janezic et al, , 2020Rodriguez et al, 2019;Tkalec et al, 2019). However, the study of C. difficile in the environment is still in its early stages with unknowns in many parts of the world.…”

“…In our 1‐year study to investigate if C. difficile is being imported into the hospital via contaminated shoe soles, RT 014/020 was the most common cause of CDI at our study hospital, consistent with a decade of surveillance data in Australia (Cheng et al, 2016; Collins et al, 2017; Foster et al, 2014; Hong et al, 2020). Locally, a high prevalence of C. difficile RT 014/020 has also been found in environmental samples, comprising up to 39%, 10%, 7%, 14% and 21% of C. difficile isolates from lawn, compost, root vegetables, hospital grounds and home gardens respectively (Lim et al, 2018, 2020; Moono et al, 2017; Perumalsamy et al, 2019; Shivaperumal et al, 2020). This, alongside a report that genetically diverse strains of C. difficile accounted for the majority of CDI cases (Eyre et al, 2013), formed the basis of our hypothesis that C. difficile is being imported into the hospital setting, possibly via contaminated shoe soles.…”

“…If this was the case, these strains were probably disseminated throughout Australia via community-based sources, possibly imported food. In WA, a high prevalence of C. difficile, most likely as spores, has been found in gardens (Shivaperumal et al, 2020), lawns (Moono et al, 2017), gardening composts and mulches (Lim et al, 2020), hospital grounds (Perumalsamy et al, 2019) and on root vegetables (Lim et al, 2018). It is believed these spores have been disseminated widely in the community following decades of using manure from production animals, with a high C. difficile prevalence rate (50%-70%; Knight et al, 2013Knight et al, , 2014, in both agriculture and horticulture.…”

Esculin hydrolysis negative and TcdA-only producing strains of Clostridium (Clostridioides) difficile from the environment in Western Australia

“…There have been reports of overlapping ribotypes (RTs) of C. difficile found in animals and humans (Anderson et al, 2017; Jhung et al, 2008) suggestive of zoonotic transmission (Jhung et al, 2008; Rupnik, 2007). The application of compost and manure containing C. difficile to gardens has led to the dissemination of C. difficile in the domestic environment (Dharmasena & Jiang, 2018; Shivaperumal et al, 2020), and contamination of vegetables (Lim et al, 2018a; Metcalf et al, 2010). Also, shoe soles are likely to carry C. difficile from gardens of all types into the built environment including healthcare systems (Janezic et al, 2018; Shivaperumal et al, 2020).…”

“…In a recent study of home gardens in Perth, Western Australia (WA), 17 strains of C. difficile were recovered that failed to produce black colonies on C. difficile ChromID™ agar (Shivaperumal et al, 2020). The objective of the present study was to further characterize these strains phenotypically and genotypically.…”