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Fecal Microbiota Transplantation for Recurrent C Difficile Infection: Ready for Prime Time?

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Fecal Microbiota Transplantation for Recurrent C Difficile Infection: Ready for Prime Time? REVIEW CME EDUCATIONAL OBJECTIVE: Readers will be aware of an effective yet little-used treatment for recurrent CREDIT Clostridium difficile infection MARKUS D. AGITO, MD ASHISH ATREJA, MD, MPH, FACP MAGED K. RIZK, MD Department of Medicine, Director, Informatics for Research, Quality Improvement Officer, Digestive Disease Akron General Medical Center, Outcomes and Quality, Assistant Professor, Institute, Cleveland Clinic; Assistant Professor, Akron, OH Division of Gastroenterology, Cleveland Clinic Lerner College of Medicine of Mount Sinai School of Medicine, Case Western Reserve University, New York, NY Cleveland, OH Fecal microbiota transplantation for recurrent C difficile infection: Ready for prime time? ■■ ABSTRACT f you had a serious disease, would you I agree to an alternative treatment that was Recurrent Clostridium difficile infection has been a major cheap, safe, and effective—but seemed dis- challenge for patients and clinicians. Recurrence of infec- gusting? Would you recommend it to patients? tion after treatment with standard antibiotics is becom- Such a disease is recurrent Clostridium dif- ing more common with the emergence of more-resistant ficile infection, and such a treatment is fecal strains of C difficile. Fecal microbiota transplantation is an microbiota transplantation—instillation of alternative treatment for recurrent C difficile infection, but blenderized feces from a healthy donor (ide- ally, the patient’s spouse or “significant other”) it is not yet widely used. into the patient’s colon to restore a healthy ■■ KEY POINTS population of bacteria.1,2 The rationale behind this procedure is simple: antibiotics and other Fecal microbiota transplantation involves instilling gut factors disrupt the normal balance of the co- microbiota from a healthy donor into the diseased gut of lonic flora, allowing C difficile to proliferate, a patient who has recurrent or recalcitrant episodes of but the imbalance can be corrected by reintro- 1 diarrhea despite antibiotic treatment for C difficile infec- ducing the normal flora. tion. The instillation can be done via nasogastric tube, In this article, we will review how recurrent C difficile infection occurs and the importance of endoscope, or enema. the gut microbiota in resisting colonization with this pathogen. We will also describe the protocol Donor screening is necessary to prevent transmission of used for fecal microbiota transplantation. communicable diseases to the recipient. ■ C DIFFICILE INFECTION OFTEN RECURS Recently published studies indicate that this procedure is effective for treating recurrent C difficile infection. Ran- C difficile is the most common cause of hospi- domized clinical trials to assess its efficacy and safety are tal-acquired diarrhea and an important cause underway. of morbidity and death in hospitalized pa- tients.3,4 The cost of this infection is estimated to be more than $1.1 billion per year and its The field of microbiota therapy is rapidly progressing. incidence is rising, partly because of the emer- More physicians are learning to embrace the concept gence of more-virulent strains that make treat- of fecal microbiota transplantation, and patients are ment of recurrent infection more difficult.5,6 beginning to overcome the “yuck factor” and accept its C difficile infection is characterized by di- benefits. arrhea associated with findings suggestive of pseudomembranous colitis or, in fulminant 7 doi:10.3949/ccjm.80a.12110 cases, ileus or megacolon. Recurrent C difficile CLEVELAND CLINIC JOURNAL OF MEDICINE VOLUME 80 • NUMBER 2 FEBRUARY 2013 101 Downloaded from www.ccjm.org on September 27, 2021. For personal use only. All other uses require permission. FECAL MICROBIOTA TRANSPLANTATION TABLE 1 CDC practice guidelines for treating Clostridium difficile infection CLINICAL DEFINITION SupportiVE CLINICAL data RECOMMENDED TREATMENT Initial episode, White blood cell (WBC) count Metronidazole 500 mg three times per mild or moderate ≤ 15,000 cells/mL day by mouth for 10–14 days Initial episode, WBC count ≥ 15,000 cells/mL Vancomycin 125 mg four times per day severe Serum creatinine ≥ 1.5 times by mouth for 10–14 days baseline Initial episode, Severe C difficile infection com- Vancomycin 500 mg four times per day severe, complicated, plicated with hypotension, shock, by mouth or nasogastric tube, plus or fulminant ileus, or megacolon metronidazole 500 mg every 8 hours intravenously If complete ileus, consider adding rectal instillation of vancomycin First recurrence Same as for initial episode Second recurrence Vancomycin in a tapered and/or pulsed regimen ADAptED FROM COhEN Sh, GERDING DN, JOhNSON S, Et AL; SOCIEtY FOR hEALthCARE EpIDEMIOLOGY OF AMERICA; INFECtIOUS DISEASES SOCIEtY OF AMERICA. CLINICAL PRACTICE GUIDELINES FOR CLOSTRIDIUM DIFFICILE INFECtION IN ADULtS: 2010 UpDAtE BY thE SOCIEtY FOR hEALthCARE EpIDEMI- OLOGY OF AMERICA (ShEA) AND thE INFECtIOUS DISEASES SOCIEtY OF AMERICA (IDSA). INFECt CONtROL hOSp EpIDEMIOL 2010; 31:431–455. COpYRIGht 2010, UNIVERSItY OF ChICAGO pRESS. infection is defined as the return of symptoms and tolevamer (a novel polymer that binds C 7 14 within 8 weeks after successful treatment. difficile toxins). C difficile is C difficile produces two types of toxins. TABLE 1 summarizes the treatment regimen the most Toxin A is an enterotoxin, causing increased for C difficile infection in adults, based on clin- intestinal permeability and fluid secretion, ical practice guidelines from the US Centers common cause while toxin B is a cytotoxin, causing intense for Disease Control and Prevention (CDC).7 of hospital- colonic inflammation. People who have a acquired poor host immune response to these toxins ■ THE NORMAL GUT MICROBIOTA tend to develop more diarrhea and colonic in- KEEPS PATHOGENS OUT diarrhea and an flammation.8 important cause A more virulent strain of C difficile has Immediately after birth, the sterile human gut emerged. Known as BI/NAP1/027, this strain becomes colonized by a diverse community of of morbidity is resistant to quinolones, and it also produces microorganisms.15 This gut microbiota per- and death a binary toxin that has a partial gene deletion forms various functions, such as synthesizing that allows for increased production of toxins vitamin K and vitamin B complex, helping A and B in vitro.9,10 More cases of severe and digest food, maintaining the mucosal integrity recurrent C difficile infection have been asso- of the gut, and priming the mucosal immune ciated with the increasing number of people response to maintain homeostasis of commen- infected with this hypervirulent strain.9,10 sal microbiota.16 C difficile infection recurs in about 20% to However, the most important role of the 30% of cases after antibiotic treatment for it, gut microbiota is “colonization resistance” or usually within 30 days, and the risk of a sub- preventing exogenous or potentially patho- sequent episode doubles after two or more genic organisms from establishing a colony occurrences.10,11 Metronidazole (Flagyl) and within the gut.17 It involves competition for vancomycin are the primary treatments; alter- nutrients and occupation of binding sites on native treatments include fidaxomicin (Difi- the gut epithelium by indigenous flora.16 Other cid),10 rifaximin (Xifaxan),12 nitazoxanide,13 factors such as the mucosal barrier, salivation, 102 CLEVELAND CLINIC JOURNAL OF MEDICINE VOLUME 80 • NUMBER 2 FEBRUARY 2013 Downloaded from www.ccjm.org on September 27, 2021. For personal use only. All other uses require permission. AGITO AND COLLEAGUES M Treating recurrent Clostridium difficile infection by restoring healthy intestinal flora The normal healthy gut teems with bacteria, Antibiotics but most of them are benign or even beneficial in ways we are only beginning to appreciate, eg, keeping out opportunistic pathogens such as Clostridium difficile. Antibiotic therapy disrupts the normal population of bacteria, paradoxically allowing colonization by C difficile. C difficile spores Development of Resolution C difficile infection of symptoms Antibiotics Antibiotic therapy for C difficile infection suppresses active infection, but the organism can form resistant spores. In addition, Recurrence antibiotics further disrupt the normal intestinal flora. As a result, C difficile infection often recurs. Donor fecal sample Fecal microbiota transplantation involves instilling fecal material from a healthy donor to restore the normal C difficile spores remain intestinal flora. CCF Medical Illustrator: Beth Halasz ©2013 FIGURE 1 CLEVELAND CLINIC JOURNAL OF MEDICINE VOLUME 80 • NUMBER 2 FEBRUARY 2013 103 Downloaded from www.ccjm.org on September 27, 2021. For personal use only. All other uses require permission. FECAL MICROBIOTA TRANSPLANTATION swallowing, gastric acidity, desquamation of in a process known as transfaunation.24 Fecal mucosal membrane cells, intestinal motility, microbiota transplantation was first performed and secretion of antibodies also play major in humans in the late 1950s in patients with roles in colonization resistance.17 fulminant pseudomembranous colitis that did not respond to standard antibiotic therapy for ■ ANTIBIOTICS DISRUPT THE GUT FLORA C difficile infection.25 Since then, a number of case reports and case series have described in- Physical or chemical injuries (the latter by an- stillation of donor stool via nasogastric tube,26 timicrobial or antineoplastic agents, eg) may via colonoscope,27–31 and via enema.32 Regard- disrupt the gut microbiota. In this situation, less of the
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