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Published in: Current Oncology Reports 7/2020

01-07-2020 | Melanoma | Melanoma (RJ Sullivan, Section Editor)

Gut Microbiome Modulation Via Fecal Microbiota Transplant to Augment Immunotherapy in Patients with Melanoma or Other Cancers

Authors: Jennifer L. McQuade, Gabriel O. Ologun, Reetakshi Arora, Jennifer A. Wargo

Published in: Current Oncology Reports | Issue 7/2020

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Abstract

Purpose of Review

We review emerging evidence regarding the impact of gut microbes on antitumor immunity, and ongoing efforts to translate this in clinical trials.

Recent Findings

Pre-clinical models and human cohort studies support a role for gut microbes in modulating overall immunity and immunotherapy response, and numerous trials are now underway exploring strategies to modulate gut microbes to enhance responses to cancer therapy. This includes the use of fecal microbiota transplant (FMT), which is being used to treat patients with Clostridium difficile infection among other non-cancer indications. The use of FMT is now being extended to modulate gut microbes in patients being treated with cancer immunotherapy, with the goal of enhancing responses and/or to ameliorate toxicity. However, significant complexities exist with such an approach and will be discussed herein.

Summary

Data from ongoing studies of FMT in cancer will provide critical insights for optimization of this approach.
Literature
3.
go back to reference Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ. Dysbiosis of the gut microbiota in disease. Microb Ecol Heal Dis Co-Action Publishing. 2015;26. Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ. Dysbiosis of the gut microbiota in disease. Microb Ecol Heal Dis Co-Action Publishing. 2015;26.
4.
go back to reference Garrett WS. Cancer and the microbiota. Science. 2015. p. 80–6. Garrett WS. Cancer and the microbiota. Science. 2015. p. 80–6.
5.
7.
go back to reference Jenq RR, Taur Y, Devlin SM, Ponce DM, Goldberg JD, Ahr KF, et al. Intestinal blautia is associated with reduced death from graft-versus-host disease. Biol Blood Marrow Transplant. Elsevier Inc. 2015;21:1373–83.CrossRef Jenq RR, Taur Y, Devlin SM, Ponce DM, Goldberg JD, Ahr KF, et al. Intestinal blautia is associated with reduced death from graft-versus-host disease. Biol Blood Marrow Transplant. Elsevier Inc. 2015;21:1373–83.CrossRef
8.
go back to reference Shono Y, Docampo MD, Peled JU, Perobelli SM, Velardi E, Tsai JJ, et al. Increased GVHD-related mortality with broad-spectrum antibiotic use after allogeneic hematopoietic stem cell transplantation in human patients and mice. Sci Transl Med. 2016 [cited 2020 Jan 8];8:339ra71. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27194729. Shono Y, Docampo MD, Peled JU, Perobelli SM, Velardi E, Tsai JJ, et al. Increased GVHD-related mortality with broad-spectrum antibiotic use after allogeneic hematopoietic stem cell transplantation in human patients and mice. Sci Transl Med. 2016 [cited 2020 Jan 8];8:339ra71. Available from: http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​27194729.
9.
go back to reference • Taur Y, Jenq RR, Perales MA, Littmann ER, Morjaria S, Ling L, et al. The effects of intestinal tract bacterial diversity on mortality following allogeneic hematopoietic stem cell transplantation. Blood. American Society of Hematology; 2014;124:1174–82. This paper was the first to demonstrate a potential role of the gut microbiome in cancer outcomes in a human cohort. • Taur Y, Jenq RR, Perales MA, Littmann ER, Morjaria S, Ling L, et al. The effects of intestinal tract bacterial diversity on mortality following allogeneic hematopoietic stem cell transplantation. Blood. American Society of Hematology; 2014;124:1174–82. This paper was the first to demonstrate a potential role of the gut microbiome in cancer outcomes in a human cohort.
10.
go back to reference Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillère R, Hannani D, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science (80- ). 2013;342:971–6.CrossRef Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillère R, Hannani D, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science (80- ). 2013;342:971–6.CrossRef
11.
12.
go back to reference •• Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science (80- ). American Association for the Advancement of Science; 2015;350:1084–9. These papers were the first. •• Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science (80- ). American Association for the Advancement of Science; 2015;350:1084–9. These papers were the first.
13.
go back to reference •• Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets T V, et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science. 2018 [cited 2019 Sep 17];359:97–103. Available from: http://www.ncbi.nlm.nih.gov/pubmed/29097493. These papers were the first. •• Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets T V, et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science. 2018 [cited 2019 Sep 17];359:97–103. Available from: http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​29097493. These papers were the first.
14.
go back to reference •• Matson V, Fessler J, Bao R, Chongsuwat T, Zha Y, Alegre ML, et al. The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science (80- ). American Association for the Advancement of Science; 2018;359:104–8. These papers were the first. •• Matson V, Fessler J, Bao R, Chongsuwat T, Zha Y, Alegre ML, et al. The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science (80- ). American Association for the Advancement of Science; 2018;359:104–8. These papers were the first.
15.
go back to reference •• Routy B, Le Chatelier E, Derosa L, Duong CPM, Alou MT, Daillère R, et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science (80- ). American Association for the Advancement of Science; 2018;359:91–7. These papers were the first. •• Routy B, Le Chatelier E, Derosa L, Duong CPM, Alou MT, Daillère R, et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science (80- ). American Association for the Advancement of Science; 2018;359:91–7. These papers were the first.
16.
go back to reference Chaput N, Lepage P, Coutzac C, Soularue E, Le Roux K, Monot C, et al. Baseline gut microbiota predicts clinical response and colitis in metastatic melanoma patients treated with ipilimumab. Ann Oncol Off J Eur Soc Med Oncol. 2017 [cited 2020 Jan 8];28:1368–79. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28368458. Chaput N, Lepage P, Coutzac C, Soularue E, Le Roux K, Monot C, et al. Baseline gut microbiota predicts clinical response and colitis in metastatic melanoma patients treated with ipilimumab. Ann Oncol Off J Eur Soc Med Oncol. 2017 [cited 2020 Jan 8];28:1368–79. Available from: http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​28368458.
17.
go back to reference Frankel AE, Coughlin LA, Kim J, Froehlich TW, Xie Y, Frenkel EP, et al. Metagenomic shotgun sequencing and unbiased metabolomic profiling identify specific human gut microbiota and metabolites associated with immune checkpoint therapy efficacy in melanoma patients. Neoplasia (US). Neoplasia Press, Inc. 2017;19:848–55.CrossRef Frankel AE, Coughlin LA, Kim J, Froehlich TW, Xie Y, Frenkel EP, et al. Metagenomic shotgun sequencing and unbiased metabolomic profiling identify specific human gut microbiota and metabolites associated with immune checkpoint therapy efficacy in melanoma patients. Neoplasia (US). Neoplasia Press, Inc. 2017;19:848–55.CrossRef
18.
go back to reference McQuade JL, Daniel CR, Helmink BA, Wargo JA. Modulating the microbiome to improve therapeutic response in cancer. Lancet Oncol. Lancet Publishing Group; 2019. p. e77–91. McQuade JL, Daniel CR, Helmink BA, Wargo JA. Modulating the microbiome to improve therapeutic response in cancer. Lancet Oncol. Lancet Publishing Group; 2019. p. e77–91.
19.
go back to reference Van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, De Vos WM, et al. Duodenal infusion of donor feces for recurrent clostridium difficile. N Engl J Med Massachussetts Medical Society. 2013;368:407–15.CrossRef Van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, De Vos WM, et al. Duodenal infusion of donor feces for recurrent clostridium difficile. N Engl J Med Massachussetts Medical Society. 2013;368:407–15.CrossRef
20.
go back to reference McDonald LC, Gerding DN, Johnson S, Bakken JS, Carroll KC, Coffin SE, 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. Oxford University Press. 2018:e1–48. McDonald LC, Gerding DN, Johnson S, Bakken JS, Carroll KC, Coffin SE, 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. Oxford University Press. 2018:e1–48.
22.
go back to reference Zmora N, Zilberman-Schapira G, Suez J, Mor U, Dori-Bachash M, Bashiardes S, et al. Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell. 2018 [cited 2020 Jan 8];174:1388-1405.e21. Available from: http://www.ncbi.nlm.nih.gov/pubmed/30193112. Zmora N, Zilberman-Schapira G, Suez J, Mor U, Dori-Bachash M, Bashiardes S, et al. Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell. 2018 [cited 2020 Jan 8];174:1388-1405.e21. Available from: http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​30193112.
24.
go back to reference Lewis BB, Buffie CG, Carter RA, Leiner I, Toussaint NC, Miller LC, et al. Loss of microbiota-mediated colonization resistance to Clostridium difficile infection with oral vancomycin compared with metronidazole. J Infect Dis. Oxford University Press; 2015 [cited 2020 Feb 17];212:1656–65. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25920320. Lewis BB, Buffie CG, Carter RA, Leiner I, Toussaint NC, Miller LC, et al. Loss of microbiota-mediated colonization resistance to Clostridium difficile infection with oral vancomycin compared with metronidazole. J Infect Dis. Oxford University Press; 2015 [cited 2020 Feb 17];212:1656–65. Available from: http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​25920320.
26.
go back to reference Kao D, Roach B, Silva M, Beck P, Rioux K, Kaplan GG, et al. Effect of oral capsule– vs colonoscopy-delivered fecal microbiota transplantation on recurrent Clostridium difficile infection: a randomized clinical trial. JAMA. American Medical Association. 2017;318:1985–93.CrossRef Kao D, Roach B, Silva M, Beck P, Rioux K, Kaplan GG, et al. Effect of oral capsule– vs colonoscopy-delivered fecal microbiota transplantation on recurrent Clostridium difficile infection: a randomized clinical trial. JAMA. American Medical Association. 2017;318:1985–93.CrossRef
28.
go back to reference Yalchin M, Segal JP, Mullish BH, Quraishi MN, Iqbal TH, Marchesi JR, et al. Gaps in knowledge and future directions for the use of faecal microbiota transplant in the treatment of inflammatory bowel disease. Therap Adv Gastroenterol. SAGE Publications Ltd; 2019 [cited 2020 Feb 17];12:1756284819891038. Available from: http://www.ncbi.nlm.nih.gov/pubmed/31803254. Yalchin M, Segal JP, Mullish BH, Quraishi MN, Iqbal TH, Marchesi JR, et al. Gaps in knowledge and future directions for the use of faecal microbiota transplant in the treatment of inflammatory bowel disease. Therap Adv Gastroenterol. SAGE Publications Ltd; 2019 [cited 2020 Feb 17];12:1756284819891038. Available from: http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​31803254.
29.
go back to reference Shanahan F, Quigley EMM. Manipulation of the microbiota for treatment of IBS and IBD—challenges and controversies. Gastroenterology WB Saunders. 2014;146:1554–63.CrossRef Shanahan F, Quigley EMM. Manipulation of the microbiota for treatment of IBS and IBD—challenges and controversies. Gastroenterology WB Saunders. 2014;146:1554–63.CrossRef
30.
go back to reference Paramsothy S, Kamm MA, Kaakoush NO, Walsh AJ, van den Bogaerde J, Samuel D, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet Lancet Publishing Group. 2017;389:1218–28.CrossRef Paramsothy S, Kamm MA, Kaakoush NO, Walsh AJ, van den Bogaerde J, Samuel D, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet Lancet Publishing Group. 2017;389:1218–28.CrossRef
33.
go back to reference Kump P, Wurm P, Gröchenig HP, Wenzl H, Petritsch W, Halwachs B, et al. The taxonomic composition of the donor intestinal microbiota is a major factor influencing the efficacy of faecal microbiota transplantation in therapy refractory ulcerative colitis. Aliment Pharmacol Ther. Blackwell Publishing Ltd; 2018 [cited 2020 Feb 17];47:67–77. Available from: http://doi.wiley.com/10.1111/apt.14387 Kump P, Wurm P, Gröchenig HP, Wenzl H, Petritsch W, Halwachs B, et al. The taxonomic composition of the donor intestinal microbiota is a major factor influencing the efficacy of faecal microbiota transplantation in therapy refractory ulcerative colitis. Aliment Pharmacol Ther. Blackwell Publishing Ltd; 2018 [cited 2020 Feb 17];47:67–77. Available from: http://​doi.​wiley.​com/​10.​1111/​apt.​14387
34.
go back to reference Moayyedi P, Surette MG, Kim PT, Libertucci J, Wolfe M, Onischi C, et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology. W.B. Saunders. 2015;149:102–109.e6.CrossRef Moayyedi P, Surette MG, Kim PT, Libertucci J, Wolfe M, Onischi C, et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology. W.B. Saunders. 2015;149:102–109.e6.CrossRef
35.
go back to reference Vermeire S, Joossens M, Verbeke K, Wang J, Machiels K, Sabino J, et al. Donor species richness determines faecal microbiota transplantation success in inflammatory bowel disease. J Crohns Colitis. Oxford University Press; 2016 [cited 2020 Feb 17];10:387–94. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26519463. Vermeire S, Joossens M, Verbeke K, Wang J, Machiels K, Sabino J, et al. Donor species richness determines faecal microbiota transplantation success in inflammatory bowel disease. J Crohns Colitis. Oxford University Press; 2016 [cited 2020 Feb 17];10:387–94. Available from: http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​26519463.
36.
go back to reference Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–31.CrossRef Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–31.CrossRef
37.
go back to reference Vrieze A, Van Nood E, Holleman F, Salojärvi J, Kootte RS, Bartelsman JFWM, et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. W.B. Saunders. 2012;143. Vrieze A, Van Nood E, Holleman F, Salojärvi J, Kootte RS, Bartelsman JFWM, et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. W.B. Saunders. 2012;143.
38.
go back to reference Kootte RS, Levin E, Salojärvi J, Smits LP, Hartstra AV, Udayappan SD, et al. Improvement of insulin sensitivity after lean donor feces in metabolic syndrome is driven by baseline intestinal microbiota composition. Cell Metab. Cell Press. 2017;26:611–619.e6.CrossRef Kootte RS, Levin E, Salojärvi J, Smits LP, Hartstra AV, Udayappan SD, et al. Improvement of insulin sensitivity after lean donor feces in metabolic syndrome is driven by baseline intestinal microbiota composition. Cell Metab. Cell Press. 2017;26:611–619.e6.CrossRef
42.
43.
go back to reference Freitag TL, Hartikainen A, Jouhten H, Sahl C, Meri S, Anttila V-J, et al. Minor effect of antibiotic pre-treatment on the engraftment of donor microbiota in fecal transplantation in mice. Front Microbiol. 2019;10:2685.CrossRef Freitag TL, Hartikainen A, Jouhten H, Sahl C, Meri S, Anttila V-J, et al. Minor effect of antibiotic pre-treatment on the engraftment of donor microbiota in fecal transplantation in mice. Front Microbiol. 2019;10:2685.CrossRef
44.
go back to reference Baruch E, Youngester Y OR. Fecal microbiota transplantation (FMT) and re-induction of anti-PD-1 therapy in refractory metastatic melanoma patients—preliminary results from a phase I clinical trial (NCT 03353402) AACR Annual Meeting. Atlanta, Georgia; 2019. Baruch E, Youngester Y OR. Fecal microbiota transplantation (FMT) and re-induction of anti-PD-1 therapy in refractory metastatic melanoma patients—preliminary results from a phase I clinical trial (NCT 03353402) AACR Annual Meeting. Atlanta, Georgia; 2019.
45.
go back to reference Maleki S, Lenehan J BJ. Combination of fecal microbiota transplantation from healthy donors with anti-PD1 immunotherapy in treatment-naïve advanced or metastatic melanoma patients. National Harbor, MD; 2019. Maleki S, Lenehan J BJ. Combination of fecal microbiota transplantation from healthy donors with anti-PD1 immunotherapy in treatment-naïve advanced or metastatic melanoma patients. National Harbor, MD; 2019.
46.
go back to reference Wang Y, Wiesnoski DH, Helmink BA, Gopalakrishnan V, Choi K, DuPont HL, et al. Fecal microbiota transplantation for refractory immune checkpoint inhibitor-associated colitis. Nat Med Nature Publishing Group. 2018;24:1804–8.CrossRef Wang Y, Wiesnoski DH, Helmink BA, Gopalakrishnan V, Choi K, DuPont HL, et al. Fecal microbiota transplantation for refractory immune checkpoint inhibitor-associated colitis. Nat Med Nature Publishing Group. 2018;24:1804–8.CrossRef
47.
go back to reference Geller LT, Barzily-Rokni M, Danino T, Jonas OH, Shental N, Nejman D, et al. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Science (80- ). American Association for the Advancement of Science. 2017;357:1156–60.CrossRef Geller LT, Barzily-Rokni M, Danino T, Jonas OH, Shental N, Nejman D, et al. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Science (80- ). American Association for the Advancement of Science. 2017;357:1156–60.CrossRef
48.
go back to reference Riquelme E, Zhang Y, Zhang L, Montiel M, Zoltan M, Dong W, et al. Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell. Cell Press. 2019;178:795–806.e12.CrossRef Riquelme E, Zhang Y, Zhang L, Montiel M, Zoltan M, Dong W, et al. Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell. Cell Press. 2019;178:795–806.e12.CrossRef
49.
go back to reference Ma C, Han M, Heinrich B, Fu Q, Zhang Q, Sandhu M, et al. Gut microbiome–mediated bile acid metabolism regulates liver cancer via NKT cells. Science (80- ). American Association for the Advancement of Science. 2018:360. Ma C, Han M, Heinrich B, Fu Q, Zhang Q, Sandhu M, et al. Gut microbiome–mediated bile acid metabolism regulates liver cancer via NKT cells. Science (80- ). American Association for the Advancement of Science. 2018:360.
50.
go back to reference Philips CA, Pande A, Shasthry SM, Jamwal KD, Khillan V, Chandel SS, et al. Healthy donor fecal microbiota transplantation in steroid-ineligible severe alcoholic hepatitis: a pilot study. Clin Gastroenterol Hepatol. 2017 [cited 2019 Nov 26];15:600–2. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27816755. Philips CA, Pande A, Shasthry SM, Jamwal KD, Khillan V, Chandel SS, et al. Healthy donor fecal microbiota transplantation in steroid-ineligible severe alcoholic hepatitis: a pilot study. Clin Gastroenterol Hepatol. 2017 [cited 2019 Nov 26];15:600–2. Available from: http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​27816755.
51.
go back to reference Bajaj JS, Kassam Z, Fagan A, Gavis EA, Liu E, Cox IJ, et al. Fecal microbiota transplant from a rational stool donor improves hepatic encephalopathy: a randomized clinical trial. Hepatology. John Wiley and Sons Inc. 2017;66:1727–38.CrossRef Bajaj JS, Kassam Z, Fagan A, Gavis EA, Liu E, Cox IJ, et al. Fecal microbiota transplant from a rational stool donor improves hepatic encephalopathy: a randomized clinical trial. Hepatology. John Wiley and Sons Inc. 2017;66:1727–38.CrossRef
52.
go back to reference Ren Y-D, Ye Z-S, Yang L-Z, Jin L-X, Wei W-J, Deng Y-Y, et al. Fecal microbiota transplantation induces hepatitis B virus e-antigen (HBeAg) clearance in patients with positive HBeAg after long-term antiviral therapy. Hepatology. 2017 [cited 2019 Nov 26];65:1765–8. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28027582. Ren Y-D, Ye Z-S, Yang L-Z, Jin L-X, Wei W-J, Deng Y-Y, et al. Fecal microbiota transplantation induces hepatitis B virus e-antigen (HBeAg) clearance in patients with positive HBeAg after long-term antiviral therapy. Hepatology. 2017 [cited 2019 Nov 26];65:1765–8. Available from: http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​28027582.
53.
go back to reference Helmink B, Gopalakrishnan V, Khan A et al. Variation of the gut microbiome of complete responders to immune checkpoint blockade and healthy individuals—implications for clinical trial design. SITC. 2018; National H:115. Helmink B, Gopalakrishnan V, Khan A et al. Variation of the gut microbiome of complete responders to immune checkpoint blockade and healthy individuals—implications for clinical trial design. SITC. 2018; National H:115.
54.
go back to reference Maier L, Pruteanu M, Kuhn M, Zeller G, Telzerow A, Anderson EE, et al. Extensive impact of non-antibiotic drugs on human gut bacteria. Nature Nature Publishing Group. 2018;555:623–8.CrossRef Maier L, Pruteanu M, Kuhn M, Zeller G, Telzerow A, Anderson EE, et al. Extensive impact of non-antibiotic drugs on human gut bacteria. Nature Nature Publishing Group. 2018;555:623–8.CrossRef
55.
go back to reference Cho I, Blaser MJ. The human microbiome: AT the interface of health and disease. Nat Rev Genet. 2012:260–70. Cho I, Blaser MJ. The human microbiome: AT the interface of health and disease. Nat Rev Genet. 2012:260–70.
56.
go back to reference McDonald D, Hyde E, Debelius JW, Morton JT, Gonzalez A, Ackermann G, et al. American gut: an open platform for citizen science microbiome research. mSystems. American Society for Microbiology; 2018;3. McDonald D, Hyde E, Debelius JW, Morton JT, Gonzalez A, Ackermann G, et al. American gut: an open platform for citizen science microbiome research. mSystems. American Society for Microbiology; 2018;3.
57.
go back to reference Thompson S, Guetterman H, Taylor A, Bogner A, Martin D, Farrell JJ, et al. Dietary predictors of fecal microbiota transplantation success. J Acad Nutr Diet. Elsevier BV. 2016;116:A76.CrossRef Thompson S, Guetterman H, Taylor A, Bogner A, Martin D, Farrell JJ, et al. Dietary predictors of fecal microbiota transplantation success. J Acad Nutr Diet. Elsevier BV. 2016;116:A76.CrossRef
Metadata
Title
Gut Microbiome Modulation Via Fecal Microbiota Transplant to Augment Immunotherapy in Patients with Melanoma or Other Cancers
Authors
Jennifer L. McQuade
Gabriel O. Ologun
Reetakshi Arora
Jennifer A. Wargo
Publication date
01-07-2020
Publisher
Springer US
Published in
Current Oncology Reports / Issue 7/2020
Print ISSN: 1523-3790
Electronic ISSN: 1534-6269
DOI
https://doi.org/10.1007/s11912-020-00913-y

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