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S41467-021-22302-0.Pdf ARTICLE https://doi.org/10.1038/s41467-021-22302-0 OPEN Microbiota-based markers predictive of development of Clostridioides difficile infection Matilda Berkell 1,46, Mohamed Mysara 1,2,46, Basil Britto Xavier 1,46, Cornelis H. van Werkhoven 3, Pieter Monsieurs2,45, Christine Lammens1, Annie Ducher4, Maria J. G. T. Vehreschild 5,6,7, Herman Goossens1, ✉ Jean de Gunzburg 4, Marc J. M. Bonten3,8, Surbhi Malhotra-Kumar 1 & the ANTICIPATE study group* Antibiotic-induced modulation of the intestinal microbiota can lead to Clostridioides difficile 1234567890():,; infection (CDI), which is associated with considerable morbidity, mortality, and healthcare- costs globally. Therefore, identification of markers predictive of CDI could substantially contribute to guiding therapy and decreasing the infection burden. Here, we analyze the intestinal microbiota of hospitalized patients at increased CDI risk in a prospective, 90-day cohort-study before and after antibiotic treatment and at diarrhea onset. We show that patients developing CDI already exhibit significantly lower diversity before antibiotic treat- ment and a distinct microbiota enriched in Enterococcus and depleted of Ruminococcus, Blautia, Prevotella and Bifidobacterium compared to non-CDI patients. We find that antibiotic treatment-induced dysbiosis is class-specific with beta-lactams further increasing enter- ococcal abundance. Our findings, validated in an independent prospective patient cohort developing CDI, can be exploited to enrich for high-risk patients in prospective clinical trials, and to develop predictive microbiota-based diagnostics for management of patients at risk for CDI. 1 Laboratory of Medical Microbiology, Vaccine & Infectious Disease Institute, University of Antwerp, Wilrijk, Belgium. 2 Microbiology Unit, Interdisciplinary Biosciences, Belgian Nuclear Research Centre, SCK–CEN, Mol, Belgium. 3 Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands. 4 Da Volterra, Paris, France. 5 Department of Internal Medicine, Center for Integrated Oncology Aachen Bonn Cologne Duesseldorf, University of Cologne, Cologne, Germany. 6 German Centre for Infection Research (DZIF), partner site Bonn-Cologne, Cologne, Germany. 7 Department of Internal Medicine, Infectious Diseases, University Hospital Frankfurt, Goethe University Frankfurt, Frankfurt am Main, Germany. 8 Department of Medical Microbiology, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands. 45Present address: Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium. 46These authors contributed equally: Matilda Berkell, Mohamed ✉ Mysara, Basil Britto Xavier. *A list of authors and their affiliations appears at the end of the paper. email: [email protected] NATURE COMMUNICATIONS | (2021) 12:2241 | https://doi.org/10.1038/s41467-021-22302-0 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-021-22302-0 lostridioides difficile is the most common cause of infec- Results C tious antibiotic-associated diarrhea (AAD) and is the Study population and design. The ANTICIPATE study recruited pathogen responsible for the largest number of 1007 patients of which 1002 provided rectal swabs at D1 and 848 healthcare-associated infections world-wide1–3. C. difficile infec- at D6 (Fig. 1). Of the 135 patients who developed diarrhea during tion (CDI) is characterized by watery stool accompanied by a period of 90 days following study inclusion, 15 were diagnosed toxin-mediated inflammation of the bowel where primary risk with CDI, as described in van Werkhoven et al.29 Stool samples factors include hospitalization, age, colonization by toxigenic from 33 of the 135 patients with diarrhea, including 6 patients C. difficile, and most importantly, antibiotic exposure where use diagnosed with CDI, collected at the occurrence of the first of fluoroquinolones (FQNs), clindamycin, carbapenems, cepha- diarrheal episode (S1) were available for analysis (Fig. 1, Table 1). losporins, and penicillins combined with beta-lactamase inhibi- Following 16S rRNA gene sequencing, 945 and 775 rectal swab tors (PBLs) are associated with increased CDI risk4–9. However, samples collected at D1 and D6, respectively, and S1 samples markers predictive of CDI or AAD development are as yet from 32 diarrheic patients (including stools from 6 CDI patients) lacking. Such markers could be utilized to stratify patients into passed data pre-processing and quality filtering criteria and were different risk categories and to enrich patient populations for analyzed further. Demographics of the 945 patients included in clinical trials assessing preventive measures against or ther- this study are detailed in Table 1. In the studied population, 390 apeutics for CDI. patients received antibiotic treatment with drugs belonging to one Patients suffering from CDI, as well as from other forms of of the following classes of broad-spectrum antibiotics: PBLs, other AAD harbor a disrupted intestinal microbiota characterized by beta-lactam antibiotics (OBLs), and FQNs (Table 1). reduced diversity and elevated levels of Enterococcus alongside Influence of baseline characteristics—gender, country of origin, reduced levels of members of the Bacteroidetes phylum, the and age by decades—on the fecal microbiome of the 945 patients Lachnospiraceae and Ruminococcaceae families, and Prevotella was assessed at D1 (Supplementary Table 1). Certain differences spp. during disease manifestation10–20. 16S rRNA gene profiling in both alpha and beta diversity were observed in the microbiota, provides a useful method for studying changes in microbial namely when patients were stratified by countries of origin composition. More importantly, it might allow identification of (Supplementary Results, Supplementary Table 1, and Supple- microbial markers predictive of the risk of CDI development. mentary Fig. 1). However, the aim of this study was to identify Although the microbial composition at CDI onset has been well- biomarkers predictive of CDI that were robust enough to studied, the pre-CDI microbiota remains largely unexplored. To transcend country, diet, and gender differences in the intestinal our knowledge, only one prospective study has investigated microbiota. Therefore, patients were not stratified by baseline microbial composition as a potential predictor of CDI18,21. This characteristics. single-center Canadian study18, part of a larger clinical study assessing CDI risk factors21, demonstrated that the absence or High-resolution 16S rRNA profiling defines C. difficile pre- reduction in Clostridiales, namely members of Clostridiales valence. Upon OTU clustering using a 97% cut-off, a single OTU Incertae Sedis XI, in the intestinal microbiota was associated classified as Clostridium XI was identified in 556 of the 945 with an increased risk of CDI18. Collateral damage on the (58.8%) patient samples at D1. High-resolution analysis of this microbiota induced by antibiotic treatment has been further OTU by oligotyping revealed two distinct types of raw reads, one shown to result in reduced alpha diversity, as well as an increase corresponding to C. difficile and the other to Clostridium bartlettii in the presence of antibiotic resistance genes, and long-lasting (also known as Intestenibacter bartlettii30), a known anaerobic effects ranging from weeks to years depending on the – occupant of the human intestine31 (Supplementary Results). antibiotic22 25. Several small studies in healthy adults have Oligotyping identified C. difficile in 51 patients (5.40%) at D1 investigated specific short-term changes induced by antibiotics, – with an average relative abundance of 0.82% (SD = 2.67, Fig. 2a). often in combination with multiple compounds25 28. None of Of these, four patients developed CDI within 1–3 days of the these, however, link antibiotic-induced dysbiosis to development D1 sampling (i.e., study inclusion). Relative abundance of C. of CDI. difficile at D1 was slightly higher in the four CDI patients (1.72%, In this multi-center, observational, prospective study, we SD = 2.18) than in the 47 patients who did not develop CDI investigated the intestinal microbiota of hospitalized patients aged within the 90-day study period (0.74%, SD = 2.70). All four CDI 50 years and above in 34 hospitals across six European countries patients underwent treatment with metronidazole and/or vanco- prior to antibiotic therapy with the aim of identifying robust mycin between the D1 and D6 sampling time-points and in two microbial markers predictive of CDI and AAD development patients, C. difficile was not detected at D6. utilizing 16S rRNA gene profiling combined with a high- Of the 945 studied patients, 737 provided both D1 and resolution sequence typing approach. Furthermore, longitudinal D6 samples. C. difficile was detected in 50 patients at D6 (6.78%) perturbations induced by different antibiotic classes were studied at a 2.5-fold higher average relative abundance (2.02%, SD = in relation to the CDI-specific and AAD-specific microbiota. Here 6.14) compared to D1 (Fig. 2b). Only 13 patients carried C. we show that patients developing CDI exhibit significantly lower difficile at both sampling time-points. C. difficile was detected in microbial diversity prior to antibiotic treatment and a distinct all six analyzed stools originating from patients with confirmed microbiota enriched in Enterococcus and depleted of Rumino- CDI at an average relative abundance
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