Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-26T21:38:49.777Z Has data issue: false hasContentIssue false
  • English
  • Français

A systematic review of economic evaluation in fecal microbiota transplantation

Published online by Cambridge University Press:  24 January 2020

Thomas Stalder ,
Nathalie Kapel ,
Sophie Diaz ,
Frédéric Grenouillet ,
Stéphane Koch ,
Samuel Limat ,
Franck Daval ,
Lucine Vuitton  and
Virginie Nerich
Thomas Stalder
Affiliation:
Department of Pharmacy, University Hospital of Besançon, Besançon, France
Nathalie Kapel
Affiliation:
Department of Coprology, Pitié-Salpêtrière University Hospital, Paris, France
Sophie Diaz
Affiliation:
Department of Pharmacy, University Hospital of Besançon, Besançon, France
Frédéric Grenouillet
Affiliation:
Department of Parasitology and Mycology, University Hospital of Besançon, Besançon, France
Stéphane Koch
Affiliation:
Department of Gastroenterology, University Hospital of Besançon, Besançon, France
Samuel Limat
Affiliation:
Department of Pharmacy, University Hospital of Besançon, Besançon, France INSERM, EFS BFC, UMR1098, University of Bourgogne Franche-Comté, Besançon, France
Franck Daval
Affiliation:
University Library, University of Franche-Comté, Besançon, France
Lucine Vuitton
Affiliation:
Department of Gastroenterology, University Hospital of Besançon, Besançon, France
Virginie Nerich*
Affiliation:
Department of Pharmacy, University Hospital of Besançon, Besançon, France INSERM, EFS BFC, UMR1098, University of Bourgogne Franche-Comté, Besançon, France
*
Author for correspondence: Virginie Nerich, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Background:

Fecal microbiota transplantation (FMT) is an effective therapy in recurrent Clostridium difficile infection (rCDI). It is only recommended for this indication by European and American guidelines. Other indications of FMT are being studied, such as inflammatory bowel disease (IBD), and they have shown promising results.

Objectives:

To identify and review published FMT-related economic evaluations (EEs) to assess their quality and the economic impact of FMT in the treatment of these diseases.

Data sources:

The systematic literature research was conducted in both PubMed and Cochrane to identify EEs published before July 1, 2019.

Study eligibility criteria:

Articles were included if they concerned FMT (whatever the disease and its line of treatment), if they reported full or partial EEs, and if they were written in English. Articles were excluded if they did not concern FMT; if they did not report an EE; or if they were a systematic review, editorial, comment, letter to the editor, practice point, or poster.

Methods:

A measurement tool, AMSTAR, was used to optimize the quality of this systematic review. Based on the CHEERS checklist, data were identified and extracted from articles. The quality of each EE was assessed using the Drummond checklist.

Results:

Overall, 9 EEs were included: all EEs were full evaluations and 8 were cost-utility analyses (CUAs). All EEs had a Drummond score ≥ 7, which indicated high quality. All CUAs related to rCDI and IBD concluded that FMT was cost-effective compared with other reference treatments, at a threshold ≤$50,000/QALY. One EE about initial CDI showed that FMT was dominated by metronidazole.

Conclusions:

Despite a limited number of EEs, FMT seems to be a promising and cost-effective treatment for rCDI. More EE studies on other diseases like IBD are necessary to address FMT efficiency for new indications. Therefore, our systematic review provides a framework for healthcare decision making.

Type
Review
Information
Infection Control & Hospital Epidemiology , Volume 41 , Issue 4 , April 2020 , pp. 458 - 466
Copyright
© 2020 by The Society for Healthcare Epidemiology of America. All rights reserved

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ramai, D, Zakhia, K, Ofosu, A, Ofori, E, Reddy, M. Fecal microbiota transplantation: donor relation, fresh or frozen, delivery methods, cost-effectiveness. Ann Gastroenterol 2019;32:30–38.Google ScholarPubMed
Reigadas Ramírez, E, Bouza, ES. Economic burden of Clostridium difficile infection in European countries. Adv Exp Med Biol 2018;1050:1–12.CrossRefGoogle ScholarPubMed
Wiegand, PN, Nathwani, D, Wilcox, MH, Stephens, J, Shelbaya, A, Haider, S. Clinical and economic burden of Clostridium difficile infection in Europe: a systematic review of healthcare-facility–acquired infection. J Hosp Infect 2012;81:1–14.CrossRefGoogle ScholarPubMed
Mathias, F, Curti, C, Montana, M, Bornet, C, Vanelle, P. Management of adult Clostridium difficile digestive contaminations: a literature review. Eur J Clin Microbiol Infect Dis 2019;38:209–231.CrossRefGoogle ScholarPubMed
Cohen, SH, Gerding, DN, Johnson, S, et al.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 2010;31:431–455.CrossRefGoogle Scholar
Surawicz, CM, Brandt, LJ, Binion, DG, et al.Guidelines for diagnosis, treatment, and prevention of Clostridium difficile infections. Am J Gastroenterol 2013;108:478–498.CrossRefGoogle ScholarPubMed
Hocquart, M, Lagier, J-C, Cassir, N, et al.Early fecal microbiota transplantation improves survival in severe Clostridium difficile infections. Clin Infect Dis 2018;66:645–650.CrossRefGoogle ScholarPubMed
van Beurden, YH, de Groot, PF, van Nood, E, Nieuwdorp, M, Keller, JJ, Goorhuis, A. Complications, effectiveness, and long term follow-up of fecal microbiota transfer by nasoduodenal tube for treatment of recurrent Clostridium difficile infection. United Eur Gastroenterol J 2017;5:868–879.CrossRefGoogle ScholarPubMed
Debast, SB, Bauer, MP, Kuijper, EJ, European Society of Clinical Microbiology and Infectious Diseases. European Society of Clinical Microbiology and Infectious Diseases: update of the treatment guidance document for Clostridium difficile infection. Clin Microbiol Infect 2014;20 suppl 2:1–26.CrossRefGoogle ScholarPubMed
McDonald, LC, Gerding, DN, Johnson, S, et al.Clinical practice guidelines for Clostridium difficile infection in adults and children: 2017 update by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA). Clin Infect Dis 2018;66:e1–e48.CrossRefGoogle Scholar
Cammarota, G, Ianiro, G, Tilg, H, et al.European consensus conference on faecal microbiota transplantation in clinical practice. Gut 2017;66:569–580.CrossRefGoogle ScholarPubMed
Suskind, DL, Brittnacher, MJ, Wahbeh, G, et al.Fecal microbial transplant effect on clinical outcomes and fecal microbiome in active Crohn’s disease. Inflamm Bowel Dis 2015;21:556–563.CrossRefGoogle ScholarPubMed
Cao, Y, Zhang, B, Wu, Y, Wang, Q, Wang, J, Shen, F. The value of fecal microbiota transplantation in the treatment of ulcerative colitis patients: a systematic review and meta-analysis. Gastroenterol Res Pract 2018;2018:5480961.CrossRefGoogle ScholarPubMed
Kang, Y, Cai, Y. Gut microbiota and obesity: implications for fecal microbiota transplantation therapy. Horm Athens Greece 2017;16:223–234.CrossRefGoogle ScholarPubMed
Kakihana, K, Fujioka, Y, Suda, W, et al.Fecal microbiota transplantation for patients with steroid-resistant acute graft-versus-host disease of the gut. Blood 2016;128:2083–2088.CrossRefGoogle ScholarPubMed
Cui, B, Feng, Q, Wang, H, et al.Fecal microbiota transplantation through mid-gut for refractory Crohn’s disease: safety, feasibility, and efficacy trial results. J Gastroenterol Hepatol 2015;30:51–58.CrossRefGoogle ScholarPubMed
He, Z, Li, P, Zhu, J, et al.Multiple fresh fecal microbiota transplants induces and maintains clinical remission in Crohn’s disease complicated with inflammatory mass. Sci Rep 2017;7.Google ScholarPubMed
Loftus, EV, Sandborn, WJ. Epidemiology of inflammatory bowel disease. Gastroenterol Clin North Am 2002;31:1–20.CrossRefGoogle ScholarPubMed
Yu, AP, Cabanilla, LA, Wu, EQ, Mulani, PM, Chao, J. The costs of Crohn’s disease in the United States and other Western countries: a systematic review. Curr Med Res Opin 2008;24:319–328.Google ScholarPubMed
Ding, X, Li, Q, Li, P, et al.Long-term safety and efficacy of fecal microbiota transplant in active ulcerative colitis. Drug Saf 2019;42:869–880.CrossRefGoogle ScholarPubMed
Sood, A, Mahajan, R, Singh, A, et al.Role of faecal microbiota transplantation for maintenance of remission in patients with ulcerative colitis: a pilot study. J Crohns Colitis 2019;13:1311–1317.CrossRefGoogle ScholarPubMed
Costello, SP, Hughes, PA, Waters, O, et al.Effect of fecal microbiota transplantation on 8-week remission in patients with ulcerative colitis: a randomized clinical trial. JAMA 2019;321:156–164.CrossRefGoogle ScholarPubMed
Moutinho, BD, Baima, JP, Rigo, FF, et al.Fecal microbiota transplantation in refractory ulcerative colitis—a case report. J Int Med Res 2019;47:1072–1079.CrossRefGoogle ScholarPubMed
Gupta, S, Allen-Vercoe, E, Petrof, EO. Fecal microbiota transplantation: in perspective. Ther Adv Gastroenterol 2016;9:229–239.CrossRefGoogle Scholar
van Nood, E, Vrieze, A, Nieuwdorp, M, et al.Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 2013;368:407–415.CrossRefGoogle ScholarPubMed
Youngster, I, Mahabamunuge, J, Systrom, HK, et al.Oral, frozen fecal microbiota transplant (FMT) capsules for recurrent Clostridium difficile infection. BMC Med 2016;14:134.CrossRefGoogle ScholarPubMed
Staley, C, Hamilton, MJ, Vaughn, BP, et al.Successful resolution of recurrent clostridium difficile infection using freeze-dried, encapsulated fecal microbiota; pragmatic cohort study. Am J Gastroenterol 2017;112:940–947.CrossRefGoogle ScholarPubMed
Cheminet, G, Kapel, N, Bleibtreu, A, et al.Faecal microbiota transplantation with frozen capsules for relapsing Clostridium difficile infections: the first experience from 15 consecutive patients in France. J Hosp Infect 2018;100:148–151.CrossRefGoogle ScholarPubMed
Kao, D, Roach, B, Silva, M, et al.Effect of oral capsule- vs colonoscopy-delivered fecal microbiota transplantation on recurrent Clostridium difficile infection: a randomized clinical trial. JAMA 2017;318:1985–1993.CrossRefGoogle ScholarPubMed
Enforcement policy regarding investigational new drug requirements for use of fecal microbiota for transplantation to treat Clostridium difficile infection not responsive to standard therapies. US Food and Drug Administration website. https://www.fda.gov/regulatory-information/search-fda-guidance-documents/enforcement-policy-regarding-investigational-new-drug-requirements-use-fecal-microbiota-0. Published 2019. Accessed July 1, 2019.Google Scholar
Guidance document: Fecal microbiota therapy used in the treatment of Clostridium difficile infection not responsive to conventional therapies. Health Canada website. https://www.canada.ca/en/health-canada/services/drugs-health-products/biologics-radiopharmaceuticals-genetic-therapies/applications-submissions/guidance-documents/regulation-fecal-microbiota-therapy-treatment-difficile-infections.html. Published 2015. Accessed July 1, 2019.Google Scholar
Megerlin, F, Fouassier, E. Fecal microbiota transplantation in France: what applicable law? Ann Pharm Fr 2014;72:363–374.CrossRefGoogle ScholarPubMed
Greenberg, D, Earle, C, Fang, C-H, Eldar-Lissai, A, Neumann, PJ. When is cancer care cost-effective? A systematic overview of cost-utility analyses in oncology. J Natl Cancer Inst 2010;102:82–88.CrossRefGoogle Scholar
Frederix, GWJ, Severens, JL, Hövels, AM, Raaijmakers, JAM, Schellens, JHM. The cloudy crystal ball of cost-effectiveness studies. Value Health J Int Soc Pharmacoecon Outcomes Res 2013;16:1100–1102.CrossRefGoogle Scholar
Cochrane Handbook for Systematic Reviews of Interventions. Cochrane website. https://handbook-5-1.cochrane.org/Updated March 2011. Accessed July 1, 2019.Google Scholar
Choices in methods for economic evaluation. Public Health Assessment Haute Autorité de Santé. Department of Economics and Public Health Assessment website. https://www.has-sante.fr/upload/docs/application/pdf/2012-10/choices_in_methods_for_economic_evaluation.pdf. Published 2012. Accessed December 27, 2019.Google Scholar
Whitehead, SJ, Ali, S. Health outcomes in economic evaluation: the QALY and utilities. Br Med Bull 2010;96:5–21.CrossRefGoogle ScholarPubMed
Shea, BJ, Grimshaw, JM, Wells, GA, et al.Development of AMSTAR: a measurement tool to assess the methodological quality of systematic reviews. BMC Med Res Method 2007;7:10.CrossRefGoogle ScholarPubMed
Husereau, D, Drummond, M, Petrou, S, et al.Consolidated Health Economic Evaluation Reporting Standards (CHEERS)—explanation and elaboration: a report of the ISPOR Health Economic Evaluation Publication Guidelines Good Reporting Practices Task Force. Value Health J Int Soc Pharmacoecon Outcomes Res 2013;16:231–250.CrossRefGoogle ScholarPubMed
Federal Reserve Bank. G.5 Release—Foreign Exchange Rates, November 01, 2016. Federal Reserve Bank website. https://www.federalreserve.gov/releases/g5/20161101/. Published 2016. Accessed July 1, 2019.Google Scholar
Drummond, MF, Sculpher, MJ, Claxton, K, Stoddart, GL, Torrance, GW. Methods for the Economic Evaluation of Health Care Programmes. London: Oxford University Press; 2015.Google Scholar
Nerich, V, Saing, S, Gamper, EM, et al.Cost-utility analyses of drug therapies in breast cancer: a systematic review. Breast Cancer Res Treat 2016;159:407–424.CrossRefGoogle ScholarPubMed
Gonzalez-Perez, JG. Developing a scoring system to quality assess economic evaluations. Eur J Health Econ 2002;3:131–136.CrossRefGoogle ScholarPubMed
Lapointe-Shaw, L, Tran, KL, Coyte, PC, et al.Cost-effectiveness analysis of six strategies to treat recurrent Clostridium difficile infection. PloS One 2016;11:e0149521.CrossRefGoogle ScholarPubMed
Zhang, T, Xiang, J, Cui, B, et al.Cost-effectiveness analysis of fecal microbiota transplantation for inflammatory bowel disease. Oncotarget 2017;8:88894–88903.CrossRefGoogle ScholarPubMed
Baro, E, Galperine, T, Denies, F, et al.Cost-effectiveness analysis of five competing strategies for the management of multiple recurrent community-onset Clostridium difficile infection in France. PloS One 2017;12:e0170258.CrossRefGoogle ScholarPubMed
Varier, RU, Biltaji, E, Smith, KJ, et al.Cost-effectiveness analysis of fecal microbiota transplantation for recurrent Clostridium difficile infection. Infect Control Hosp Epidemiol 2015;36:438–444.CrossRefGoogle ScholarPubMed
Merlo, G, Graves, N, Brain, D, Connelly, LB. Economic evaluation of fecal microbiota transplantation for the treatment of recurrent Clostridium difficile infection in Australia. J Gastroenterol Hepatol 2016;31:1927–1932.CrossRefGoogle ScholarPubMed
Konijeti, GG, Sauk, J, Shrime, MG, Gupta, M, Ananthakrishnan, AN. Cost-effectiveness of competing strategies for management of recurrent Clostridium difficile infection: a decision analysis. Clin Infect Dis 2014;58:1507–1514.CrossRefGoogle ScholarPubMed
Waye, A, Atkins, K, Kao, D. Cost averted with timely fecal microbiota transplantation in the management of recurrent Clostridium difficile infection in Alberta, Canada. J Clin Gastroenterol 2016;50:747–753.CrossRefGoogle ScholarPubMed
Varier, RU, Biltaji, E, Smith, KJ, et al.Cost-effectiveness analysis of treatment strategies for initial Clostridium difficile infection. Clin Microbiol Infect 2014;20:1343–1351.CrossRefGoogle ScholarPubMed
Jiang, M, Leung, N-H, Ip, M, You, JHS. Cost-effectiveness analysis of ribotype-guided fecal microbiota transplantation in Chinese patients with severe Clostridium difficile infection. PloS One 2018;13:e0201539.CrossRefGoogle ScholarPubMed
Rajasingham, R, Enns, EA, Khoruts, A, Vaughn, BP. Cost-effectiveness of treatment regimens for Clostridioides difficile infection—an evaluation of the 2018 Infectious Diseases Society of America guidelines. Clin Infect Dis 2019. pii: ciz318. doi:10.1093/cid/ciz318.Google Scholar
Sokol, H, Galperine, T, Kapel, N, et al.Faecal microbiota transplantation in recurrent Clostridium difficile infection: recommendations from the French Group of Faecal Microbiota Transplantation. Dig Liver Dis Liver 2016;48:242–247.Google Scholar
Le, P, Nghiem, VT, Mullen, PD, Deshpande, A. Cost-effectiveness of competing treatment strategies for Clostridium difficile infection: a systematic review. Infect Control Hosp Epidemiol 2018;39:412–424.CrossRefGoogle ScholarPubMed
Supplementary material: File

Stalder et al. supplementary material

Stalder et al. supplementary material 1

Download Stalder et al. supplementary material(File)
File 15.1 KB
Supplementary material: File

Stalder et al. supplementary material

Stalder et al. supplementary material 2

Download Stalder et al. supplementary material(File)
File 17.6 KB