Abstract
Background
The success of fecal microbiota transplantation (FMT) programs depends on maintaining suitable stool donors. We describe challenges recruiting and retaining universal donors in the first 2 years of an FMT clinical and research program in Toronto and identify opportunities for improvement.
Methods
A four-stage screening process is used to identify suitable FMT donors in the Microbiota Therapeutics Outcomes Program. Donor screening follows Health Canada recommendations and excludes persons with history or risk for diseases associated with dysbiosis. Donors are rescreened microbiologically approximately every 1–3 months and answer ongoing health, exposure, and dietary questionnaires.
Results
In the first 2 years of our program, 5 of 322 (1.6%) prospective stool donors passed initial screening, and only 2 (0.6%) were retained. Most prospective donors were excluded on telephone screening, at which point high BMI, medication use, and family history of relevant illness were common exclusions. No candidate was excluded because of a concerning physical examination. Microbiologic reasons for donor exclusion included carriage of Blastocystis hominis (n = 2), Helicobacter pylori (n = 2), extended spectrum beta-lactamase producing organisms (n = 1), Shiga-toxin producing Escherichia coli (n = 1), and sapovirus (n = 1). Universal donors were lost temporarily because of travel, antibiotic exposures, and transient carriage of antibiotic-resistant organisms.
Conclusions
Recruiting and retaining suitable donors for FMT is challenging because of rigorous exclusions and labour-intensive screening processes. We present considerations for efficiency in donor screening, including targeting recruitment populations, expanded website self-screening, eliminating physical examinations, and streamlining post-travel risk assessment.
Keywords: donor program, fecal microbiota transplantation, recurrent Clostridium difficile infection
Abstract
Historique
Le succès des programmes de transplantation de microbiote fécal (TMF) dépend de la rétention de donneurs fécaux appropriés. Les auteurs décrivent les difficultés à recruter et à conserver des donneurs universels dans les deux premières années d’un programme clinique et de recherche de TMF à Toronto ainsi qu’à déterminer les possibilités d’amélioration.
Méthodologie
Un processus de sélection en quatre étapes permet de déterminer les donneurs de TMF appropriés au sein du programme de résultats thérapeutiques du microbiote. La sélection des donneurs suit les recommandations de Santé Canada et exclut les personnes ayant des antécédents ou un risque de maladies associés à la dysbiose. Les donneurs reprennent une sélection microbiologique environ tous les un à trois mois et répondent à des questionnaires sur la santé, l’exposition et le régime alimentaire.
Résultats
Au cours de deux premières années du programme, cinq des 322 donneurs prospectifs de matière fécale (1,6 %) ont réussi la sélection initiale, et seulement deux (0,6 %) ont été retenus. La plupart des donneurs prospectifs ont été exclus à la sélection téléphonique; un IMC élevé, la prise de médicaments et des antécédents familiaux de maladie pertinente étaient des exclusions courantes. Aucun candidat n’a été exclu à cause d’un examen physique inquiétant. Les raisons microbiologiques d’exclure les donneurs incluaient le portage de Blastocystis hominis (n = 2), d’Helicobacter pylori (n = 2), d’organismes producteurs de bêta-lactamase à large spectre (n = 1), d’Escherichia coli producteur de la toxine de Shiga (n = 1) et du sapovirus (n = 1). Des donneurs temporaires étaient perdus temporairement à cause de voyages, d’exposition à des antibiotiques et de portage transitoire d’organismes antibiorésistants.
Conclusions
Il est difficile de recruter et de retenir des donneurs appropriés de TMF en raison des exclusions rigoureuses et des processus de dépistage fastidieux. Les auteurs présentent des considérations d’efficacité pour le dépistage des donneurs, y compris le ciblage de populations à recruter, l’autodépistage élargi dans les sites Web, l’élimination des examens physiques et la rationalisation de l’évaluation du risque après le voyage.
Mots-clés : infection récurrente à Clostridium difficile, programme de donneurs, transplantation de microbiote fécal, infection récurrente à Clostridium difficile
Fecal microbiota transplantation (FMT), the transfer of stool from a healthy, screened donor to a patient with a disease associated with imbalanced intestinal microbiota (dysbiosis), has gained popularity as a treatment for recurrent Clostridium difficile infection (RCDI). It is also increasingly being investigated for use with people with other health conditions, including obesity, hepatic encephalopathy, bipolar disorder, and carriage of antimicrobial-resistant organisms (1).
The success of FMT programs depends heavily on the ability to recruit and retain sufficient stool donors. These donors must pass rigorous screening for infectious and non-infectious diseases that may be associated with the transfer of stool from one person to another. Increasingly, FMT programs are using universal stool donors, who, once approved for donation, provide stool for FMT on an ongoing basis and at a regular frequency. This allows programs to focus resources on a small pool of donors who will reliably provide stool for the program, and it decreases the frequency of conducting initial donor screens. Even still, the requirements of universal stool donation can be a deterrent to recruitment, and FMT programs struggle to cover costs because most in Canada are currently funded through research grants and in-kind contributions from hospitals (2). We describe the challenges in recruiting and retaining donors in the first 2 years of an FMT clinical and research program in Toronto that uses universal stool donors, and we identify opportunities to improve the efficiencies of the program.
Methods
The Microbiota Therapeutics Outcomes Program (MTOP) was developed in 2016 to provide FMT to patients with RCDI and to facilitate research into other, diverse health applications of FMT in Toronto. This program began through seed funding from the University of Toronto’s Department of Medicine and in-kind contributions from the University Health Network and Sinai Health Services, where the MTOP is based.
Prospective FMT donors are recruited through paper flyers posted in downtown Toronto (in hospitals, on university campuses, and at other educational institutes in proximity to the MTOP donor centre) and through the MTOP website (http://www.mtop.ca). They undergo four successive steps of screening:
Website self-screening: All interested candidates who contact the MTOP coordinator are directed to view a brief list of questions on the MTOP website (https://mtop.ca/donor-screening-questionnaire/) that assess their ability to commit to the program and important exclusions such as age, BMI, medication use, and high-risk behaviours that are associated with acquisition of blood-borne and sexually transmitted infections. They are instructed to contact the MTOP coordinator again only if they pass the questionnaire. Donors who would otherwise pass the website screening but are using over-the-counter medications, herbal remedies, or supplements are invited to reinitiate contact with the program after completing a 6-month wash-out period of these substances with the understanding that they will remain off of them for the duration of stool donation.
Telephone screening: The MTOP coordinator confirms the website screening questions, explains the screening process in more detail, and conducts an extensive medical questionnaire to identify active and potential risk for various health problems.
In-person screening: A physical examination is conducted, anthropometric measurements are taken (height, weight, waist circumference), a psychiatric questionnaire is administered (Mini-International Neuropsychiatric Interview [MINI]), and blood testing to calculate the homeostatic model assessment–insulin resistance (HOMA–IR), a risk measure for insulin resistance, is performed (3).
Microbiologic screening: Blood, stool, and urine are tested for blood-borne, enteric, and sexually transmitted pathogens and antimicrobial-resistant enteric organisms using enteric stool culture tests available as part of routine testing. Extended testing is also conducted, including a molecular syndromic gastrointestinal panel (BioFire FilmArray Gastrointestinal Panel, bioMérieux, Saint-Laurent, QC), Chlamydia trachomatis and Neisseria gonorrhoeae molecular testing on both urine and stool specimens (Cobas® CT/NG polymerase chain reaction [PCR], Roche Diagnostics Canada, Laval, QC), and Helicobacter pylori antigen testing on stool (Premier Platinum HpSA® PLUS EIA, Meridien Bioscience, Cincinnati, OH; Table 1). Those who are found to be positive for an antimicrobial-resistant organism or enteric virus are invited to return for rescreening after completing a 3-month wash-out period.
Table 1:
Microbiologic screening of prospective donors in the Microbiota Therapeutics Outcomes Program
| Biospecimens & Assay | Pathogen |
|---|---|
| Stool | |
| Stool Helicobacter pylori antigen assay, (Premier Platinum HpSA PLUS EIA, Meridien Bioscience, Cincinnati, OH) |
|
| Molecular syndromic gastrointestinal panel (BioFire FilmArray Gastrointestinal Panel, bioMérieux, Saint-Laurent, QC) |
|
| Neisseria gonorrhoeae and Chlamydia trachomatis PCR assay (Cobas CT/NG, Roche Diagnostics Canada, Laval, QC) |
|
| Microscopic examination for ova and parasites following provincial reference laboratory protocols (https://www.publichealthontario.ca/en/laboratory-services/test-information-index) |
|
| Fecal swab | |
| Stool culture following site clinical laboratory protocols (http://www.mountsinai.on.ca/education/staff-professionals/microbiology) |
|
| Urine | |
| N. gonorrhoeae and C. trachomatis PCR assay (Cobas CT/NG, Roche Diagnostics Canada, Laval, QC) |
|
| Serum | |
| Serology following site clinical laboratory protocols (http://www.mountsinai.on.ca/education/staff-professionals/microbiology) |
|
| Serology following site provincial reference laboratory protocols (https://www.publichealthontario.ca/en/laboratory-services/test-information-index) |
|
EIEC = enteroinvasive Escherichia coli; EAEC = enteroaggreative E. coli; EPEC = enteropathogenic E. coli; ETEC = enterotoxigenic E. coli; STEC = Shiga like toxin-producing E. coli; PCR = polymerasse chain reaction; MRSA = methicillin-resistant Staphylococcus aureus; VRE = vancomycin-resistant enterococci; CPE = carbapenemase-producing Enterobacteriaceae; ESBL = extended spectrum beta-lactamases; HBsAg = hepatitis B surface antigen; IgM = immunoglobulin M; IgG = immunoglobulin G; HBcAb = hepatitis B core antibody; HCV = hepatitis C virus; HTLV = human T-cell lymphotrophic virus
The screening completed by following these four successive steps follows Health Canada’s recommendations (4) and includes additional exclusions that address the risk of non-infectious diseases potentially associated with dysbiosis. Full details on the exclusion and inclusion criteria can be found in the Supplemental Materials.
MTOP donors provide informed consent, and these activities have been approved by the institutional review boards of the University Health Network and Sinai Health Services. Approved donors are requested to provide FMT donations three to five times per week, reporting changes in health, travel history, high-risk activities, and dietary exposures to common allergens on questionnaires submitted with each stool donation. Those who report exposures to antibiotics or other medications and travel to areas where infectious diseases are endemic are required to pass a 6-month wash-out period followed by repeat microbiologic rescreening before donating again. Microbiologic rescreening occurs after a donor has provided 1,500–2,250 g of stool, which is enough stool to make 10–15 FMTs (usually every 1–3 months), or as needed depending on changes in risk activity.
Donations are processed on receipt and then frozen and held in quarantine until rescreening results are available. If rescreening results are negative, donations provided up to 2 weeks before rescreening are released. If at any time a donor is found to be positive for an antimicrobial-resistant organism or enteric virus, the donor is invited to return for repeat microbiologic screening after completing a 3-month wash-out assuming they are in good health and asymptomatic at that time. Safety aliquots are retained for each manufactured FMT filtrate in the event that a trace-back is required to investigate possible transmission of infection. Because our program is currently supported through limited research funds, a nominal incentive of $150 per 15 FMT is provided to active donors.
The success rates at each stage of donor screening and reasons for prospective donor exclusions were analyzed using descriptive statistics.
Results
Between June 1, 2016, and May 31, 2018, 322 prospective donors presented to MTOP for screening. The proportion that continued onward at each successive stage of donor screening were as follows: (1) website self-screening, 79.5% (256/322); (2) telephone screening, 7.8% (20/256); (3) in-person screening, 75.0% (15/20); and (4) microbiologic screening, 33.3% (5/15) (Figure 1). Reasons for exclusion or drop-out at each stage of screening beyond website self-screening are provided in Figure 2. Medication use, high BMI, and family history of relevant illness were the most common exclusions on telephone screening, accounting for 36%, 34%, and 11% of dropouts, respectively. Additionally, 27% of potential donors dropped out at telephone screening because they were unwilling or unable to complete donor screening or commit to the FMT donor protocols (16%) or donate 3–5 times per week (11%). No candidate was excluded as a result of concerning physical examination findings, but one individual failed because of elevated BMI as calculated by MTOP personnel and another because of an elevated HOMA–IR score. Asymptomatic carriage of enteric potential pathogens, including Blastocystis hominis (n = 2), H. pylori (n = 2), extended spectrum beta-lactamase producing organisms (ESBL) (n = 1), Shiga-toxin producing Escherichia coli (n = 1), and sapovirus (n = 1) were noted, but no blood-borne or sexually transmitted infections were detected.
Figure 1:
Number of prospective donors proceeding to the next step of donor screening in the MTOP
Excluded prospective donors included those who failed screening as well as those who were asked to be in a wash-out period and did not reconnect with MTOP and those who were in the process of being evaluated or contacted at the time of data analysis
MTOP = Microbiota Therapeutics Outcomes Program
Figure 2:
Breakdown of prospective donors who passed screening compared with those who were excluded in successive stages of prospective donor screening in the MTOP, June 1, 2016–May 31, 2018
MTOP = Microbiota Therapeutics Outcomes Program; WP = wash-out period (initiated when prospective donors had recently taken medications, vitamins, or supplements); TBC = to be contacted; TBD = to be determined at the time of data analysis
Of the five approved donors, two became active donors to the program. Of the approved but not active donors, one was lost as a result of the inability to donate regularly. One travelled internationally shortly after completing screening and was excluded because enteropathogenic E. coli was detected in the stool on rescreening. Another travelled internationally to an area with endemic Zika virus and was excluded on the basis of exposure risk. Both of these latter donors were invited to be rescreened after a wash-out period but did not follow up and do so. Of the active donors, one active donor received antibiotics for a presumed infection 3 months after starting to donate to the program, resulting in a 6-month exclusion from donating. One donor reported international travel after starting to donate to the program; after careful evaluation by two MTOP physicians of the regions visited during this travel, the donor was permitted to continue donating without rescreening. Of seven rescreening events among the two active donors, one was positive for presence of ESBL. All quarantined donations provided by this donor before this rescreening were tested for ESBL, and all were negative. These donations were then released for use.
Discussion
We describe the early experience of a multi-purpose FMT donor program supporting treatment of RCDI and multidisciplinary research into other, diverse health applications of FMT in Toronto that applied a rigorous, four-step screening program to identify suitable donors. Of 322 prospective donors evaluated over 2 years, only 5 (1.6%) passed full screening and only 2 (0.6%) became active donors. Retention of active donors was complicated by unanticipated antibiotic exposure, travel, and the need to investigate transient carriage of antibiotic-resistant enteric organisms.
International stool donor bank experiences have been published, but most have relatively small samples (<170) of prospective donors (5–12). Donor pass rates range from 2% to 37%, with the majority of programs falling in the 10%–20% range (5–12). In our program, a large proportion of prospective donors dropped out or were excluded in the initial stages of screening (website and telephone screening). We were unable to accurately account for the reasons for drop-out from website screening. However, our data reveal that 27% of prospective donors did not proceed past telephone screening because of unwillingness to complete donor screening, follow FMT donor protocols, or provide stool donations three to five times per week (Figure 3). This confirms that the screening and donation requirements for universal stool donors for FMT programs and stool banks continue to be a significant deterrent for prospective donors.
Figure 3:
Breakdown of reasons for exclusion in successive stages of prospective donor screening in the MTOP, June 1, 2016–May 31, 2018
MTOP = Microbiota Therapeutics Outcomes Program; HOMA–IR = homeostatic model assessment–insulin resistance (exclusion occurred if HOMA–IR was >2.73); MINI = Mini-International Neuropsychiatric Interview (exclusion occurred if a potential donor responded yes to any of the MINI modules); ESBL = extended-spectrum beta-lactamase producing organism
Targeting an appropriate population for FMT donor recruitment is a crucial step that determines program efficiency. The type of advertisement strategies used is frequently limited by lack of available funds, because Canadian FMT programs struggle to cover costs through research grants and in-kind contributions from hospitals (2). The location of donors is a critical criterion to consider given the need for donors to provide regular, in-person donations. Recently, a centre reported feasibility in recruiting stool donors from among blood donors, of whom 20% were eligible for stool donation (6). Although this strategy may be useful for enriching the pool of suitable donors for FMT, there is no guarantee that blood donors will be equally as motivated to donate stool to support an FMT program. Unlike blood donation programs, universal stool donor programs for FMT depend on maintaining a small pool of highly reliable donors to provide regular donations on an ongoing basis.
Our program has the added complexity of needing to target young, healthy donors who are willing to drop off fresh stool donations on a nearly daily basis. It is not clear how Canadian blood donors would view or fit these requirements. This approach would have to be further explored at the local level to determine whether it would prove beneficial for improving the efficiency of FMT donor recruitment. Similarly, allogenic living tissue donors could be targeted as potential stool donors, but it is not clear how much these different donor groups would overlap given the unique requirements for universal stool donors outlined earlier.
The breadth of donor exclusions and frequency of rescreening vary considerably among reported stool donor programs, because consensus on these criteria has not been achieved. We follow Health Canada’s guidelines for microbiologic screening of prospective FMT donors and have further expanded screening for non-infectious illnesses that are postulated to be associated with gastrointestinal dysbiosis, given the nature of the ongoing clinical trials supported by our FMT program (4). For quality assurance purposes and to reduce the risk of human error, we have chosen to bank universal donor stool screened by one consistent approach to minimize the amount of variation in our banked donor stools. Some FMT programs in Canada may be able to apply less extensive donor screening criteria for non-infectious diseases, depending on the patient populations being treated with FMT and recipients’ willingness to accept the risks.
MTOP potential donors were excluded because of asymptomatic carriage of B. hominis, H. pylori, ESBLs, Shiga-toxin producing Escherichia coli, and sapovirus. Similar to our experience, the asymptomatic presence of B. hominis, Dientamoeba fragilis, H. pylori, rotavirus, ESBL E. coli, and Shiga toxin in stool have been reported as common microbiologic exclusions of donors in other published studies (5,6,8–12). The inclusion of B. hominis as an exclusion criterion may be considered controversial given that its pathogenicity is not conclusive; however, given that we provide FMT for patients with milder or functional immunosuppression (e.g., chronic, low-dosage use of prednisone; patients on renal replacement therapy), we elected to include it. Few centres have reported on donor retention; those that have remark on travel, acute gastroenteritis, antibiotic exposure, pregnancy, and carriage of enteric pathogens on rescreening as reasons for losing donors (5,8,11), which is consistent with our experience.
In our program, self-screening accomplished by reading a brief website questionnaire was effective in eliminating prospective donors who participated in high-risk activities but ineffective in excluding those who did not meet our specified criteria for age, BMI, and medication use. Other stool banks have successfully used extensive, self-administered website screening questionnaires for prospective donors that require submission to the program before in-person assessment (7). Such an approach would increase efficiency and decrease the human resource requirement for upstream aspects of donor screening, such as telephone screening. Moreover, the active nature of providing responses to an online questionnaire may encourage prospective donors to provide more complete and accurate information. Physical examination did not reveal any signs of illness that would result in donor exclusion. Because physical examinations must be conducted by a physician or delegated regulated health professional trained in this skill, eliminating this step could also increase the efficiency of the screening process by reducing delays and costs. We have continued with physician-led physical examinations because we feel that the connection forged between prospective donors and our physicians has had a positive influence on donors’ willingness to commit to the program. It also facilitates the process of disclosing diagnoses revealed during donor screening, if the need should later arise.
Our microbiologic screening detected more asymptomatic enteric pathogen and antimicrobial-resistant organism carriage in prospective donors than anticipated. Toronto is a multicultural city and international travel hub, characteristics that may affect our prospective donors’ risks for carriage of ESBLs and parasites such as B. hominis (13). Indeed, travel within our approved donor pool resulted in the elimination of one donor because of asymptomatic carriage of enteropathogenic E. coli. The transient carriage of ESBL noted in one of our active donors without a travel history, hospitalization, or antimicrobial exposure points to the potential for acquisition of antimicrobial-resistant organisms locally in the community through food or other exposures.
The use of a multiplex molecular gastrointestinal pathogen testing panel for microbiologic donor screening proved to be high yield in detecting potential enteric pathogens that would not otherwise be isolated through traditional stool culture-based methods (enteropathogenic E. coli, shiga toxin-producing E. coli). The panel also identified common enteric viruses (e.g., sapovirus), for which testing is not routinely available in Ontario. Although our experience suggests that the use of a multiplex molecular gastrointestinal pathogen panel is helpful for FMT donor screening, we recognize that these tests have some limitations. As previously noted by others, multiplex molecular gastrointestinal pathogen panels have been developed for testing of symptomatic patients with gastroenteritis and not specifically for asymptomatic patient screening, as is done with FMT donors (12). In addition, the cost of repeated multiplex molecular gastrointestinal pathogen testing is high. These costs must be balanced against the risks of new pathogen acquisition among universal FMT donors to justify a reasonable frequency of rescreening.
We present the first published experience of a Canadian FMT donor program, highlighting challenges in donor recruitment and retention that should be noted by institutions considering providing this service. Our report is purely descriptive, but we provide useful insights into the need to tailor FMT donor programs to the patient population being treated and the local population, taking into account demographics, travel patterns, and circulating communicable diseases to adequately resource recruitment efforts. It also provides valuable data on how to improve the efficiency of FMT donor screening programs. Moving forward, we plan to streamline our website and telephone screening, liberating resources to support more effective donor recruitment and retention efforts.
Funding Statement
This work was supported by the University of Toronto, Department of Medicine Integrating Challenge Grant.
Competing Interests:
Dr. Poutanen reports receiving honoraria for involvement in advisory board and speaking events and travel reimbursement for speaking events from Merck Pharmaceuticals, advisory board honoraria from Cipher and Verity Pharmaceuticals, grants from Accelerate Diagnostics, and travel reimbursement from Copan outside the submitted work.
Ethics Approval:
These activities were approved by the institutional review boards of the University Health Network and Sinai Health Services.
Informed Consent:
MTOP donors provided informed consent.
Registry and the Registration No. of the Study/Trial:
N/A
Animal Studies:
N/A
Funding:
This work was supported by the University of Toronto, Department of Medicine Integrating Challenge Grant.
Peer Review:
This article has been peer reviewed.
References
- 1.National Institutes of Health registered trials involving fecal microbiota transplantation. https://www.clinicaltrials.gov/ct2/results?cond=fecal+microbiota+transplantation&term=&cntry=&state=&city=&dist=. (January 11, 2019).
- 2.Hota SS, Surangiwala S, Paterson AS, Coburn P, Poutanen SM; Southern Ontario Fecal Transplant (SOFT) Movement. Regional variability in fecal microbiota transplantation practices: a survey of the Southern Ontario Fecal microbiota Transplantation Movement. CMAJ Open 2018; 6(2): E184–E190. 10.9778/cmajo.20170109. Medline: [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Sheehan DV, Lecrubier Y, Sheehan KH, et al. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 1998; 59(Suppl 20):22–33. 10.1016/S0924-9338(97)83296-8. [DOI] [PubMed] [Google Scholar]
- 4.Health Canada. Guidance document: Fecal microbiota therapy used in the treatment of Clostridium difficile infection not responsive to conventional therapies. http://www.hc-sc.gc.ca/dhp-mps/consultation/biolog/fecal_microbiota-bacterio_fecale-eng.php. (January 11, 2019).
- 5.Craven LJ, Parvathy S, Tat-Ko J, Burton JP, Silverman MS. Extended screening costs associated with selecting donors for fecal microbiota transplantation for treatment of metabolic syndrome-associated diseases. Open Forum Infect Dis 2017; 4(4):ofx243. 10.1093/ofid/ofx243. Medline: [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Dahl Jorgensen SM, Erikstrup C, Dinh KM, Lemming LE, Dahlerup JF, Hvas CL. Recruitment of feces donors among blood donors: results from an observational cohort study. Gut Microbes 2018; 9(6):540–50. 10.1080/19490976.2018.1458179. Medline: [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Openbiome. Openbiome Quality and Safety Program. 2018. http://www.openbiome.org/safety/. (January 11, 2019).
- 8.Terveer EM, van Beurden YH, Goorhuis et al. How to: establish and run a stool bank. Clin Microbiol Infect 2017; 23(12): 924–30. 10.1016/j.cmi.2017.05.015. Medline: [DOI] [PubMed] [Google Scholar]
- 9.Costello SP, Tucker EC, La Brooy J, Schoeman MN, Andrews JM. Establishing a fecal microbiota transplant service for the treatment of Clostridium difficile infection. Clin Infect Dis 2016; 62(7): 908–14. 10.1093/cid/civ994. Medline: [DOI] [PubMed] [Google Scholar]
- 10.Paramsothy S, Borody TJ, Lin E, et al. Donor recruitment for fecal microbiota transplantation. Inflamm Bowel Dis 2015;21(7): 1600–6. 10.1097/MIB.0000000000000405. Medline: [DOI] [PubMed] [Google Scholar]
- 11.Tariq R, Weatherly R, Kammer P, Pardi DS, Khanna S. Donor screening experience for fecal microbiota transplantation in patients with recurrent C. difficile infection. J Clin Gastroenterol 2018;52(2):146–150. Medline:. [DOI] [PubMed] [Google Scholar]
- 12.Woodworth MH, Neish EM, Miller NS, et al. Laboratory testing of donors and stool samples for fecal microbiota transplantation for recurrent Clostridium difficile infection. J Clin Microbiol 2017; 55(4): 1002–10. 10.1128/JCM.02327-16. Medline: [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Peirano G, Gregson DB, Kuhn S, Vanderkooi OG, Nobrega DB, Pitout JDD. Rates of colonization with extended-spectrum beta-lactamase-producing Escherichia coli in Canadian travelers returning from South Asia: a cross-sectional assessment. CMAJ Open 2017; 5(4): E850–55. 10.9778/cmajo.20170041. Medline: [DOI] [PMC free article] [PubMed] [Google Scholar]