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Journal of Pediatric Gastroenterology & Nutrition:
doi: 10.1097/MPG.0b013e318292fa0d
Original Articles: Gastroenterology

Safety, Tolerability, and Clinical Response After Fecal Transplantation in Children and Young Adults With Ulcerative Colitis

Kunde, Sachin*; Pham, Angela*; Bonczyk, Sarah; Crumb, Teri*; Duba, Meg*; Conrad, Harold Jr*; Cloney, Deborah*; Kugathasan, Subra

Free Access
Continued Medical Education
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Author Information

*Spectrum Health, Helen DeVos Children's Hospital, Grand Rapids

Michigan State University, Grand Rapids, MI

Emory University School of Medicine, Atlanta, GA.

Address correspondence and reprint requests to Sachin Kunde, MD, MPH, Pediatric Gastroenterology, 35 Michigan St NE, Ste 4150, Grand Rapids, MI 49503 (e-mail: Sachin.Kunde@helendevoschildrens.org).

Received 5 March, 2013

Accepted 18 March, 2013

This article has been developed as a Journal CME Activity by NASPGHAN. Visit http://www.naspghan.org/wmspage.cfm?parm1=361 to view instructions, documentation, and the complete necessary steps to receive CME credit for reading this article.

www.clinicaltrials.gov registration number: NCT01560819.

The study was funded by a Helen DeVos Children's Hospital Foundation Grant.

The authors report no conflicts of interest.

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Abstract

Background and Objective: Colonic dysbiosis contributes to the development of colonic inflammation in ulcerative colitis (UC). Fecal microbial transplantation (FMT) is being proposed as a novel treatment for UC because it can eliminate dysbiosis; however, no prospective data exist. We initiated a pilot study to evaluate feasibility and safety of FMT in children with UC.

Methods: Ten children, 7 to 21 years of age, with mild-to-moderate UC (pediatric UC activity index [PUCAI] between 15 and 65) received freshly prepared fecal enemas daily for 5 days. Data on tolerability, adverse events, and disease activity were collected during FMT and weekly for 4 weeks after FMT. Clinical response was defined as decrease in PUCAI by >15, and decrease in PUCAI to <10 was considered clinical remission.

Results: No serious adverse events were noted. Mild (cramping, fullness, flatulence, bloating, diarrhea, and blood in stool) to moderate (fever) adverse events were self-limiting. One subject could not retain fecal enemas. Average tolerated enema volume by remaining 9 subjects was 165 mL/day. After FMT, 7 of the 9 (78%) subjects showed clinical response within 1 week, 6 of the 9 (67%) subjects maintained clinical response at 1 month, and 3 of the 9 (33%) subjects achieved clinical remission at 1 week after FMT. Median PUCAI significantly improved after FMT (P = 0.03) compared with the baseline.

Conclusions: Fecal enemas were feasible and tolerated by children with UC. Adverse events were acceptable, self-limiting, and manageable by subjects. FMT indicated efficacy in the treatment of UC.

See “Medical Stool: The Future of Treatment for Inflammatory Bowel Disease?” by Davidovics and Sylvester on page 583.

Ulcerative colitis (UC) is a chronic, devastating inflammatory bowel disease affecting the colon without a medical cure. UC is characterized by decreased prevalence of protective bacteria and concomitant increase in detrimental bacteria in the colon (1). The colonic microbiome in patients with UC has decreased richness and diversity (2,3) and is dysfunctional (4) (dysbiosis). Colonic inflammation in UC is hypothesized to result from an inappropriate activation of the mucosal innate immune system because of dysbiosis in genetically susceptible individuals.

Medications (aminosalicylic acid preparations, steroids, immunomodulators, and biologics such as anti-tumor necrosis factor-α [TNF-α]) used to treat UC have significant adverse effects. These medical options focus on limiting the colonic inflammation without addressing the dysbiosis itself. Probiotics, for example, VSL#3, have shown some usefulness in the treatment of UC (5); however, not all probiotic formulations contain the same species, their efficacy may be strain specific, and understanding of their mechanism of action in the complex gastrointestinal (GI) microbiome is lacking.

Fecal microbial transplantation (FMT) is being proposed as a novel therapeutic approach specifically to modulate dysbiosis and thereby decrease colonic inflammation in UC. Recent evidence suggests that FMT, the infusion of fecal preparation from a healthy donor into the GI tract of a patient, is capable of altering the gut microbiome of the new host (6,7). Since the first case report nearly 2 decades ago (8), FMT has been used sporadically to treat inflammatory bowel diseases (9), with claims of clinical (10) and endoscopic remission (11). Although abundant data support the possible use of FMT in the treatment of recurrent Clostridium difficile infection with a success rate of nearly 90% (7,12,13), limited reports are available on its role in treating UC. No prospective data exist on the applicability of FMT in patients with UC.

Children represent a considerable population affected by UC because approximately 25% of patients are diagnosed during their childhood (younger than 20 years). The psychological turmoil associated with UC appears to be profound in children, who seem less able than older patients to adapt and cope with their disease (14,15). Therefore, as an initial step in understanding the role of FMT in UC, we conducted a phase I clinical trial evaluating feasibility, safety, and tolerability of FMT in children with UC. We also measured the effect of FMT on clinical disease activity in this population to understand its potential efficacy.

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METHODS

Study Oversight

The study was approved by the Spectrum Health institutional review board. Informed consent was obtained from the participants (subjects/parents and donors) at the time of enrollment. When used to treat a disease, human stool constitutes a drug and a biologic. Therefore, an investigational new drug approval (IND#14993) was obtained from the US Food and Drug Administration to use FMT for treating UC. The study was registered at www.clinicaltrials.gov before enrolling any participants.

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Study Design

A prospective, open-label, uncontrolled, single-center pilot study was conducted at Helen DeVos Children's Hospital's outpatient gastroenterology facility. Subjects were enrolled between April and December 2012. The study was not advertised. Each subject participated in the study for 6 weeks (Fig. 1). Subjects received FMT as freshly prepared fecal retention enemas.

Figure 1
Figure 1
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Study Population
Subjects

Ten children between the ages of 7 to 21 years with mild-to-moderate UC (pediatric UC activity index [PUCAI] between 15 and 65) were enrolled prospectively. Subjects had stable disease activity and medical treatment for UC for 2 months before the enrollment. Subjects’ exclusion criteria included fulminant colitis, scheduled for abdominal surgery, pregnancy, concurrent probiotic or antibiotic use, severe anemia (hemoglobin <6 g/dL), graft-versus-host disease, immunocompromised host defined as neutropenia or history of opportunistic infection, major intraabdominal surgery within 3 months before FMT, administration of any investigational drug within 1 month before FMT, and use of anti-TNF-α medications within 2 months before FMT or its expected use within 1 month after FMT. Subjects’ ongoing treatment for UC was not changed. None of the subjects had concurrent C difficile infection.

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Donors

Healthy adults (older than 18 years of age) selected by subjects from their family members or close friends were used as donors. Donor exclusion criteria were guided by our IND, the American Association of Blood Bank Donor History Questionnaire version 1.1, and the recommendations from the American Gastroenterological Association (16). Donor exclusion criteria included positive response on the donor screening questionnaire; history of inflammatory bowel diseases, irritable bowel syndrome, chronic abdominal pain, or GI malignancy; diarrhea, blood in stool or antibiotic use within 1 month before FMT; immunocompromised, defined as taking immunosuppressive medications, history of opportunistic infection within 1 year before FMT, oral thrush, or disseminated lymphadenopathy; and abnormal donor screening tests. Donor screening tests were performed by Spectrum Health Regional Laboratory, which is certified by federal Clinical Laboratory Improvement Amendments. The donor screening laboratory values included blood tests (hepatitis A immunoglobulin [Ig]M, hepatitis B surface Ag, hepatitis B surface Ab, hepatitis B core Ab, hepatitis C Ab, Epstein-Barr virus viral capsid antigen IgM, cytomegalovirus IgM, syphilis IgG, HIV I and II enzyme-linked immunosorbent assay), and stool tests (stool culture for Salmonella, Shigella, Escherichia coli, Campylobacter, Yersinia, Vibrio, and Listeria, C difficile toxin polymerase chain reaction, ova and parasite screening, fungal smear).

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Donor Fecal Preparation

Donors produced stool samples within 6 hours before the scheduled FMT. Donors were asked to take over-the-counter stool softeners, if necessary, to produce stool samples on schedule. Donor stool was handled as a level 2 biohazard with appropriate universal precautions. On average, each donor produced a 90-g (range 70–113 g) stool sample every day, which was used for FMT. Fecal samples were blended with 250 mL sterile warm (37°C) normal saline for 1 minute using a conventional blender in a designated GI laboratory space. This blended fecal mixture was then filtered through 2 gauze pieces to remove larger sediments. Filtered fecal preparation was then divided into 4 aliquots of 60 mL each and kept in a warm water bath (37°C) until FMT was administered.

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Study Intervention

Subjects did not receive any bowel preparation (cleanout or antibiotic pretreatment) before FMT. To help relieve children's anxiety about FMT, we used audiovisual aids to keep them engaged during intervention. Subjects were put in the left lateral decubitus position with elevated hips in a designated private GI clinic room for 90 minutes for FMT intervention. Each subject received FMT as retention enema for 1 hour (60-mL enema every 15 minutes) daily for 5 days. Each 60-mL enema was infused for 5 minutes. Subjects were then asked to rotate 180° (from left lateral to right lateral position and then back to left lateral position) slowly during a 10-minute period. Although 240 mL of fecal solution was prepared for FMT, the final administered dose was dependent on the subject's comfort and willingness to proceed with the next enema, which was assessed after each enema infusion. Subjects were monitored for 30 minutes after FMT for any immediate adverse events and discharged. No antimotility drugs were used to help retain FMT.

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Safety Monitoring and Endpoints

An adverse event was defined as any untoward medical occurrence associated with FMT, whether or not related to FMT. A serious adverse event was defined as an adverse event that results in death, is life-threatening, or requires hospitalization. Adverse events were recorded during FMT and until 4 weeks after FMT using an easy-to-understand symptom diary that subjects completed. Intensity and relation of adverse events with FMT was described using Common Terminology Criteria for Adverse Events version 3.0 and Toxicity Grading Guidance from Vaccine Clinical Trials (US Food and Drug Administration, September 2007). Intensity of adverse events was classified as mild, moderate, severe, or disabling. Relation of adverse events with FMT was categorized as unrelated or possibly, probably, or definitely related to FMT. Safety reporting was in accordance with the IND requirements per the Code of Federal Regulations, Title 21 (CFR 312.32). A data safety monitoring committee was established that monitored adverse events and halting criteria after every 3 subjects completed the study to assess for patterns and rate of reported or observed complications. Halting criteria was defined as the occurrence of any serious adverse event or if ≥3 subjects experienced a similar adverse event of severe intensity that was related to FMT.

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Tolerance

Tolerance was defined as ability of subjects to retain a >60-mL enema. This volume was based on the standard mesalamine and hydrocortisone enemas volume used to treat UC. Intolerance was defined as immediate leaking of enema during administration or inability to retain enema for at least 1 hour after administration. No further FMT was performed if the subject showed intolerance for 3 consecutive days.

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Clinical Response

Clinical disease activity was measured using PUCAI (17,18), which was calculated at the enrollment, at starting FMT, and weekly for 4 weeks after FMT. We expected a mild-to-moderate improvement in UC symptoms after FMT. Therefore, clinical response was defined as a decrease in PUCAI by >15 points after FMT (17). Clinical remission was defined as decrease in PUCAI to <10. The clinical endpoint was defined as clinical response at 1 month after FMT. The data on PUCAI were collected by using an easy-to-understand symptom questionnaire, which listed symptoms of PUCAI (abdominal pain, rectal bleeding, stool consistency, number of stools, nocturnal stools, and activity limitation). To avoid investigator bias, we did not use clinical recall elicited by investigators. The questionnaire was completed by subjects based on their most recent (within last 2 days) symptoms.

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Statistical Analysis

No power calculation or sample size assessment was done for this pilot study. Data on adverse events, tolerability, and disease activity are reported as descriptive analysis. Changes in PUCAI after FMT were compared with baseline using Wilcoxon signed rank test. P value <0.05 was considered statistically significant.

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RESULTS

We received interest from patients from all over the world to participate in this study. Fifteen subjects were assessed for the eligibility to enroll in the study (Fig. 1). We enrolled all of the planned 10 subjects within 9 months of starting the study. The age of subjects ranged from 7 to 20 years (Table 1). Steroid-dependent patients continued to take the medication throughout the study period. Only 1 subject had used anti-TNF-α medications in the past. All had active disease diagnosed by colonoscopy within 6 months before the enrollment. All of the donors were first-degree relatives of subjects, except 1 subject, who identified a family friend as donor. All of the donors had negative/normal screening laboratories (blood and stool tests).

Table 1
Table 1
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Tolerance

One subject showed intolerance with immediate leaking of enemas for 3 consecutive days. The remaining 9 subjects tolerated enema volumes ranging from 75 to 240 mL (average 165 mL) without leakage. These 9 subjects tolerated FMT well because they were able to retain fecal enemas from 3 to 24 hours (average 10 hours).

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Adverse Events

Subject-reported symptoms and their relations with FMT are described in Table 2. No serious adverse events were noted. As expected, fecal enemas were associated with mild left-sided abdominal fullness. One subject reported a moderate degree of fever and chills 3 hours after FMT, which spontaneously resolved during the next 6 hours for 2 consecutive FMT days. No signs of sepsis were reported. For the remaining 3 FMT days, the use of antipyretic (acetaminophen) and antihistaminic (diphenhydramine) medications immediately after FMT prevented the development of fever. Another subject had single episode of low-grade fever (without chills or signs of sepsis) after FMT; no intervention was necessary. Owing to the temporal relation of fever with FMT and use of medications to control this symptom, fever was classified as “probably” related to FMT.

Table 2
Table 2
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Disabling hematochezia was seen in the third week after FMT (not shown in Table 2) in 1 subject (subject no. 4). Because this subject showed initial clinical response to FMT and there was a lack of immediate temporal relation with FMT, the symptom was likely because of an UC flare and unlikely from the FMT intervention. This subject responded well to corticosteroid enema therapy. Other reported symptoms that were not related to FMT included cervical lymphadenopathy (after an upper respiratory infection during follow-up period in 1 subject); lower back pain (from positioning while performing FMT in 1 subject); headache, nausea, or vomiting (baseline symptoms from concurrent medication use in 3 subjects). All of the adverse events related to FMT were self-limiting, did not require intervention from health care providers (except fever), and the majority of them were similar to subjects’ baseline symptoms of UC.

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Clinical Response

The subject who showed intolerance to FMT was not included in the clinical response evaluation. After FMT, 7 of the 9 (78%) subjects showed clinical response within 1 week. Six of the 9 subjects (67%) maintained clinical response at 1 month. Three of the 9 (33%) subjects achieved clinical remission at 1 week after FMT and were able to maintain it by 4 weeks after FMT (Fig. 2). Median PUCAI score significantly decreased after FMT (P = 0.03) compared with baseline. The decision to cease medications for UC for the subjects who achieved clinical remission after the study completion was left to their respective gastroenterologists.

Figure 2
Figure 2
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DISCUSSION

The results of this study demonstrate that performing FMT as fecal enemas is feasible; they are well tolerated and safe in children with UC. The study also indicates the potential efficacy of FMT in treating UC. We report, for the first time, that when used to mitigate a human condition, human stool constitutes a biologic, and IND approval should be obtained to perform FMT.

As reported previously (10), because of the chronic process of colonic inflammation, multiple FMT sessions may be needed to see a clinical response in UC. As such, we performed 5 FMT treatments compared with 1 (or 2) treatments required for recurrent C difficile infection (7). Multiple studies have used various bowel sterilizing preparations (antibiotics and bowel cleanout) before FMT (19,20) to help donor microbiota establish in the new host. We did not use any bowel preparation to avoid confounding of the changes in clinical response and also to avoid further discomfort to children. Upper and lower GI routes have been used to administer FMT; however, because of the vulnerable nature of our study population, we chose enema as the safest route to instill FMT. In this exploratory study, for the safety of the subjects, we excluded children with severe UC (PUCAI >65) and immunocompromised subjects (eg, taking concurrent anti-TNF-α). We did this to limit the theoretical risk of sepsis from possible translocation of new bacteria through inflamed mucosa during FMT, although no such risk has been reported yet (7,21). Further long-term follow-up studies are required to determine safety and to exclude the possibility of inadvertent transmission of disease-causing pathogens through FMT.

Limited data are available on the adverse events related to FMT. A recent study (7) evaluating the role of FMT in treating recurrent C difficile infection reported adverse events, which, similar to our study, were predominantly GI symptoms. The symptoms were short-lived, acceptable to subjects, and manageable. Symptoms (other than fever) reported by our study population were similar to the symptoms of UC, and thus could not be definitely attributed to FMT. Similar to our study, development of fever after FMT without signs of sepsis or positive blood culture has been reported in patients with UC (22). This indicates that FMT may mount a temporary systemic immune response without bacteremia and it can be prevented using antipyretic and antihistaminic medications.

Selection of 240-mL volume for FMT was based on earlier studies (10,20,23), which used colonoscopic or enema routes of FMT infusion. Administrating FMT for 1 hour with changing positions helped subjects retain large volume enemas for a longer time. The FMT enema was tolerated (>60 mL) even by the youngest subjects; however, the subject who showed intolerance was an adult. This indicates that intolerance to fecal enemas may not be dependent on age or size of the subject. The determinants of intolerance may include severity of distal colonic disease, experience with enemas, and anxiety associated with the enema.

A dramatic response to FMT seen within 1 week was not maintained by all of the subjects. We speculate that differences in the clinical response seen in our study population can be the result of severity, duration or the extent of the disease, and because of the differences in the ability to retain larger FMT volumes for longer periods. Whether patients with UC need a longer duration of FMT or multiple scheduled FMT infusions to maintain a clinical response is unknown and needs further exploration. A recent systematic review of case reports on the use of FMT in the management of inflammatory bowel diseases indicated that 76% of subjects experienced improvement in symptoms and 63% achieved clinical remission after FMT (9). In this review, 18 patients had UC without concurrent C difficile infection and 13 of these 18 (72%) patients showed clinical response after FMT. This is similar to clinical response seen in our population.

As expected with any single-center, uncontrolled study, we cannot exclude investigator or participant bias; however, every attempt was made to collect the data objectively (eg, use of symptom questionnaire) without bias by investigators. Because of financial limitations, fecal and mucosal microbial community profiling was not performed. This profiling would have been critical to determine whether the mechanism of action in FMT in the treatment of UC is similar to its use in recurrent C difficile infection (eg, reestablishing the normal microbiota (6) and increasing fecal bacteria diversity) (7). Colonoscopic disease activity or stool inflammatory markers (to support reported disease activity) was also not measured because of financial limitations and should be a part of future studies. Whether there are any implications in using adult donors for pediatric patients is unknown and should be addressed in future studies. We did not use age-matched or pediatric donors for this study because we believed it was unethical to ask a child to produce a stool on demand or to take a medication for that reason. This short-term pilot study is limited by its small sample size; therefore, studies with a larger sample size and longer follow-up period will be required to determine true efficacy of FMT in patients with UC.

Use of FMT in UC may not be as simple as its use in recurrent C difficile infection. To better understand how FMT can be used to treat UC, many unanswered questions need to be addressed. We must further investigate standardization of FMT preparation, ideal donor selection, ideal route of administration, and optimal duration or scheduling of FMT to induce and maintain a clinical response. Most important, the effects of FMT on the colonic microbiome and mucosal inflammation in UC need to be explored.

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CONCLUSIONS

FMT in the form of fecal enema is feasible and well tolerated by children and young adults with UC. Adverse events of FMT are mild to moderate, acceptable by subjects, self-limiting, and manageable. This unique biologic is potentially efficacious in treating UC.

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Acknowledgments

The authors acknowledge the Helen DeVos Children's Hospital Foundation for supporting this research, the Spectrum Health Regional Laboratory for performing donor screening, and the Center for Biologics Research and Evaluation for continued guidance for IND.

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Keywords:

fecal bacteriotherapy; fecal transplantation; ulcerative colitis

Copyright 2013 by ESPGHAN and NASPGHAN

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