Current challenges in the treatment of severe Clostridium difficile infection: early treatment potential of fecal microbiota transplantation

Yvette H van Beurden, Max Nieuwdorp, Pablo J E J van de Berg, Chris J J Mulder, Abraham Goorhuis, Yvette H van Beurden, Max Nieuwdorp, Pablo J E J van de Berg, Chris J J Mulder, Abraham Goorhuis

Abstract

Fecal microbiota transplantation (FMT) is a very effective treatment for recurrent Clostridium difficile infection (CDI). Less is known about the application of FMT as a curative treatment of severe or complicated CDI. In this review, we present and discuss evidence supporting the curative use of FMT in severe or complicated CDI. We performed a literature search in PubMed and Embase for studies on the curative use of FMT in severe or complicated CDI. In addition, we describe a patient with severe CDI not responding to initial antibiotic treatment, who was successfully treated with curative FMT. We found 23 reports (12 case reports; 11 case series) about FMT as treatment for severe or complicated CDI. The patients described all had severe or complicated CDI, did not respond to conventional CDI antibiotic treatment and received FMT as last resort treatment. Patients were treated with (sequential) FMT, whether or not followed by additional antibiotic treatment for CDI. FMT, with or without additional antibiotic CDI treatment, appears to be a promising curative treatment option in patients with severe and complicated CDI, or only complicated CDI, who do not respond sufficiently to conventional antibiotic treatment. Treatment with FMT should be considered in these patients before proceeding to emergency bowel surgery.

Keywords: colectomy; fecal microbiota transplantation (FMT); gut microbiota; severe and complicated Clostridium difficile infection (CDI); treatment.

Conflict of interest statement

Conflict of interest statement: The authors declare that there is no conflict of interest.

References

    1. Agrawal M., Aroniadis O., Brandt L., Kelly C., Freeman S., Surawicz C., et al. (2015) The long-term efficacy and safety of fecal microbiota transplant for recurrent, severe, and complicated clostridium difficile infection in 146 elderly individuals. J Clin Gastroenterol 50: 403–407.
    1. Aroniadis O., Brandt L., Greenberg A., Borody T., Kelly C., Mellow M., et al. (2015) Long-term follow-up study of fecal microbiota transplantation for severe and/or complicated clostridium difficile infection: a multicenter experience. J Clin Gastroenterol 50: 398–402.
    1. Asonuma K., Kuroki Y., Ino S., Hanamura S., Takano Y., Yamamura E., et al. (2016) Severe refractory clostridium difficile infection with good response to fecal microbiota transplantation: a case report. Nihon Shokakibyo Gakkai Zasshi 113: 55–62.
    1. Bassis C., Theriot C., Young V. (2014) Alteration of the murine gastrointestinal microbiota by tigecycline leads to increased susceptibility to clostridium difficile infection. Antimicrob Agents Chemother 58: 2767–2774.
    1. Berman L., Carling T., Fitzgerald T., Bell R., Duffy A., Longo W., et al. (2008) Defining surgical therapy for pseudomembranous colitis with toxic megacolon. J Clin Gastroenterol 42: 476–480.
    1. Berro Z., Hamdan R., Dandache I., Saab M., Karnib H., Younes M. (2016) Fecal microbiota transplantation for severe clostridium difficile infection after left ventricular assist device implantation: a case control study and concise review on the local and regional therapies. BMC Infect Dis 16: 234.
    1. Borody T., Khoruts A. (2012) Fecal microbiota transplantation and emerging applications. Nat Rev Gastroenterol Hepatol 9: 88–96.
    1. Bowden T., Jr., Mansberger A., Jr., Lykins L. (1981) Pseudomembraneous enterocolitis: mechanism for restoring floral homeostasis. Am Surg 47: 178–183.
    1. Butala P., Divino C. (2010) Surgical aspects of fulminant clostridium difficile colitis. Am J Surg 200: 131–135.
    1. Cammarota G., Ianiro G., Magalini S., Gasbarrini A., Gui D. (2015a) Decrease in surgery for clostridium difficile infection after starting a program to transplant fecal microbiota. Ann Intern Med 163: 487–488.
    1. Cammarota G., Masucci L., Ianiro G., Bibbo S., Dinoi G., Costamagna G., et al. (2015b) Randomised clinical trial: faecal microbiota transplantation by colonoscopy vs. vancomycin for the treatment of recurrent clostridium difficile infection. Aliment Pharmacol Ther 41: 835–843.
    1. Chang J., Antonopoulos D., Kalra A., Tonelli A., Khalife W., Schmidt T., et al. (2008) Decreased diversity of the fecal microbiome in recurrent clostridium difficile-associated diarrhea. J Infect Dis 197: 435–438.
    1. Cohen S., Gerding D., Johnson S., Kelly C., Loo V., Mcdonald L., et al. (2010) Clinical practice guidelines for clostridium difficile infection in adults: 2010 update by the society for healthcare epidemiology of America (Shea) and the infectious diseases society of America (Idsa). Infect Control Hosp Epidemiol 31: 431–455.
    1. Dallal R., Harbrecht B., Boujoukas A., Sirio C., Farkas L., Lee K., et al. (2002) Fulminant clostridium difficile: an underappreciated and increasing cause of death and complications. Ann Surg 235: 363–372.
    1. Earhart M. (2008) The identification and treatment of toxic megacolon secondary to pseudomembranous colitis. Dimens Crit Care Nurs 27: 249–254.
    1. Eiseman B., Silen W., Bascom G., Kauvar A. (1958) Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery 44: 854–859.
    1. Fenton S., Stephenson D., Weder C. (1974) Pseudomembranous colitis associated with antibiotic therapy - an emerging entity. Can Med Assoc J 111: 1110–1111, 1114.
    1. Feuerstadt P., Das R., Brandt L. (2014) The evolution of urban C. difficile infection (Cdi): Cdi in 2009-2011 is less severe and has better outcomes than Cdi in 2006-2008. Am J Gastroenterol 109: 1265–1276.
    1. Fischer M., Kao D., Mehta S., Martin T., Dimitry J., Keshteli A., et al. (2016) Predictors of early failure after fecal microbiota transplantation for the therapy of clostridium difficile infection: a multicenter study. Am J Gastroenterol 111: 1024–1031.
    1. Fischer M., Sipe B., Rogers N., Cook G., Robb B., Vuppalanchi R., et al. (2015) Faecal microbiota transplantation plus selected use of vancomycin for severe-complicated clostridium difficile infection: description of a protocol with high success rate. Aliment Pharmacol Ther 42: 470–476.
    1. Gallegos-Orozco J., Paskvan-Gawryletz C., Gurudu S., Orenstein R. (2012) Successful colonoscopic fecal transplant for severe acute clostridium difficile pseudomembranous colitis. Rev Gastroenterol Mex 77: 40–42.
    1. Gweon T., Kim J., Lim C., Park J., Lee D., Lee I., et al. (2016) Fecal microbiota transplantation using upper gastrointestinal tract for the treatment of refractory or severe complicated clostridium difficile infection in elderly patients in poor medical condition: the first study in an Asian country. Gastroenterol Res Pract 2016: 2687605.
    1. Hall J., Berger D. (2008) Outcome of colectomy for clostridium difficile colitis: a plea for early surgical management. Am J Surg 196: 384–388.
    1. Jeon Y., Hong N., Kim J., Park S., Kim S., Song I., et al. (2016) Fecal transplantation using a nasoenteric tube during an initial episode of severe clostridium difficile infection. Infect Chemother 48: 31–35.
    1. Johal S., Hammond J., Solomon K., James P., Mahida Y. (2004) Clostridium difficile associated diarrhoea in hospitalised patients: onset in the community and hospital and role of flexible sigmoidoscopy. Gut 53: 673–677.
    1. Johnson S. (2009) Recurrent clostridium difficile infection: a review of risk factors, treatments, and outcomes. Journal of Infection 58: 403–410.
    1. Khoruts A., Dicksved J., Jansson J., Sadowsky M. (2010) Changes in the composition of the human fecal microbiome after bacteriotherapy for recurrent clostridium difficile-associated diarrhea. J Clin Gastroenterol 44: 354–360.
    1. Koss K., Clark M., Sanders D., Morton D., Keighley M., Goh J. (2006) The outcome of surgery in fulminant clostridium difficile colitis. Colorectal Dis 8: 149–154.
    1. Lofgren E., Cole S., Weber D., Anderson D., Moehring R. (2014) Hospital-acquired clostridium difficile infections: estimating all-cause mortality and length of stay. Epidemiology 25: 570–575.
    1. Louie T., Cannon K., Denis M., Byrne B., Ward L. (2010) Quantitative real-time pcr measurement of the impact of fidaxomicin or vancomycin treatment of clostridium difficile infection on the intestinal microbiome, compared with normal controls. Clinical Microbiology and Infection 16: S166.
    1. Louie T., Emery J., Krulicki W., Byrne B., Mah M. (2009) Opt-80 eliminates clostridium difficile and is sparing of bacteroides species during treatment of C. difficile infection. Antimicrob Agents Chemother 53: 261–263.
    1. Marcos L., Gersh A., Blanchard K., Foil S., Mallini B., Farrell S., et al. (2015) Fecal transplantation to treat initial severe clostridium difficile infection with sepsis. J Miss State Med Assoc 56: 38–40.
    1. Neal M., Alverdy J., Hall D., Simmons R., Zuckerbraun B. (2011) Diverting loop ileostomy and colonic lavage: an alternative to total abdominal colectomy for the treatment of severe, complicated clostridium difficile associated disease. Ann Surg 254: 423–427; discussion 427–429.
    1. Neemann K., Eichele D., Smith P., Bociek R., Akhtari M., Freifeld A. (2012) Fecal microbiota transplantation for fulminant clostridium difficile infection in an allogeneic stem cell transplant patient. Transpl Infect Dis 14: E161–165.
    1. Patel N., Griesbach C., Dibaise J., Orenstein R. (2013) Fecal microbiota transplant for recurrent clostridium difficile infection: mayo clinic in Arizona experience. Mayo Clin Proc 88: 799–805.
    1. Pecere S., Sabatelli M., Fantoni M., Ianiro G., Gasbarrini A., Cammarota G. (2015) Letter: faecal microbiota transplantation in combination with fidaxomicin to treat severe complicated recurrent clostridium difficile infection. Aliment Pharmacol Ther 42: 1030.
    1. Potakamuri L., Turnbough L., Maheshwari A., Kantsevoy S., Ofosu A., Thuluvath P., et al. (2013) Effectiveness of fecal microbiota transplantation for the treatment of recurrent clostridium difficile infection: community hospital experience. American Journal of Gastroenterology 108: S175.
    1. Seekatz A., Rao K., Santhosh K., Young V. (2016) Dynamics of the fecal microbiome in patients with recurrent and nonrecurrent clostridium difficile infection. Genome Med 8: 47.
    1. Shin J., Ko E., Lee S., Shin J., Kim S., Kwon K., et al. (2016) Refractory pseudomembranous colitis that was treated successfully with colonoscopic fecal microbial transplantation. Intest Res 14: 83–88.
    1. Song Y., Garg S., Girotra M., Maddox C., Von Rosenvinge E., Dutta A., et al. (2013) Microbiota dynamics in patients treated with fecal microbiota transplantation for recurrent clostridium difficile infection. PLoS One 8: e81330.
    1. Surawicz C., Brandt L., Binion D., Ananthakrishnan A., Curry S., Gilligan P., et al. (2013) Guidelines for diagnosis, treatment, and prevention of clostridium difficile infections. American Journal of Gastroenterology 108: 478–498.
    1. Trubiano J., Gardiner B., Kwong J., Ward P., Testro A., Charles P. (2013) Faecal microbiota transplantation for severe clostridium difficile infection in the intensive care unit. Eur J Gastroenterol Hepatol 25: 255–257.
    1. Van Beurden Y., De Groot P., Van Nood E., Nieuwdorp M., Keller J., Goorhuis A. (2016b) Complications, effectiveness, and long term follow-up of fecal microbiota transfer by nasoduodenal tube for treatment of recurrent clostridium difficile infection. UEG journal doi:10.1177/2050640616678099
    1. Van Beurden Y., Dekkers O., Bomers M., Kaiser A., Van Houdt R., Knetsch C., et al. (2016a) An outbreak of clostridium difficile ribotype 027 associated with length of stay in the intensive care unit and use of selective decontamination of the digestive tract: a case control study. PLoS One 11: e0160778.
    1. Van Nood E., Vrieze A., Nieuwdorp M., Fuentes S., Zoetendal E., De Vos W., et al. (2013) Duodenal infusion of donor feces for recurrent clostridium difficile. N Engl J Med 368: 407–415.
    1. Wang J., Xiao Y., Lin K., Song F., Ge T., Zhang T. (2015) Pediatric severe pseudomembranous enteritis treated with fecal microbiota transplantation in a 13-month-old infant. Biomed Rep 3: 173–175.
    1. Weingarden A., Hamilton M., Sadowsky M., Khoruts A. (2013) Resolution of severe clostridium difficile infection following sequential fecal microbiota transplantation. J Clin Gastroenterol 47: 735–737.
    1. Yoon S., Brandt L. (2010) Treatment of refractory/recurrent C. difficile-associated disease by donated stool transplanted via colonoscopy: a case series of 12 patients. J Clin Gastroenterol 44: 562–566.
    1. You D., Franzos M., Holman R. (2008) Successful treatment of fulminant clostridium difficile infection with fecal bacteriotherapy. Ann Intern Med 148: 632–633.
    1. Zainah H., Hassan M., Shiekh-Sroujieh L., Hassan S., Alangaden G., Ramesh M. (2015) Intestinal microbiota transplantation, a simple and effective treatment for severe and refractory clostridium difficile infection. Dig Dis Sci 60: 181–185.

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