Fecal microbiota transplantation plus anti-PD-1 immunotherapy in advanced melanoma: a phase I trial.

Animals Mice Fecal Microbiota Transplantation / methods Immune Checkpoint Inhibitors Feces / microbiology Melanoma / therapy Immunotherapy Treatment Outcome

Journal

Nature medicine
ISSN: 1546-170X
Titre abrégé: Nat Med
Pays: United States
ID NLM: 9502015

Informations de publication

Date de publication:
08 2023
Historique:
received: 09 02 2023
accepted: 08 06 2023
medline: 17 8 2023
pubmed: 7 7 2023
entrez: 6 7 2023
Statut: ppublish

Résumé

Fecal microbiota transplantation (FMT) represents a potential strategy to overcome resistance to immune checkpoint inhibitors in patients with refractory melanoma; however, the role of FMT in first-line treatment settings has not been evaluated. We conducted a multicenter phase I trial combining healthy donor FMT with the PD-1 inhibitors nivolumab or pembrolizumab in 20 previously untreated patients with advanced melanoma. The primary end point was safety. No grade 3 adverse events were reported from FMT alone. Five patients (25%) experienced grade 3 immune-related adverse events from combination therapy. Key secondary end points were objective response rate, changes in gut microbiome composition and systemic immune and metabolomics analyses. The objective response rate was 65% (13 of 20), including four (20%) complete responses. Longitudinal microbiome profiling revealed that all patients engrafted strains from their respective donors; however, the acquired similarity between donor and patient microbiomes only increased over time in responders. Responders experienced an enrichment of immunogenic and a loss of deleterious bacteria following FMT. Avatar mouse models confirmed the role of healthy donor feces in increasing anti-PD-1 efficacy. Our results show that FMT from healthy donors is safe in the first-line setting and warrants further investigation in combination with immune checkpoint inhibitors. ClinicalTrials.gov identifier NCT03772899 .

Identifiants

DOI: 10.1038/s41591-023-02453-x PMID: 37414899
pubmed: 37414899
doi: 10.1038/s41591-023-02453-x
pii: 10.1038/s41591-023-02453-x
doi:

Substances chimiques

Immune Checkpoint Inhibitors 0

Banques de données

ClinicalTrials.gov
['NCT03772899']

Types de publication

Clinical Trial, Phase I Multicenter Study Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2121-2132

Subventions

Organisme : CIHR
ID : PJT-178341
Pays : Canada
Organisme : CIHR
ID : PJT – 156295
Pays : Canada
Organisme : CIHR
ID : MOP 389137
Pays : Canada

Commentaires et corrections

Type : CommentIn
Type : CommentIn
Type : ErratumIn

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature America, Inc.

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Auteurs

Bertrand Routy (B)

Research Center of the Centre Hospitalier de l'Université de Montréal, Montréal (CRCHUM), Montreal, Quebec, Canada.
Hematology-Oncology Division, Department of Medicine, Centre Hospitalier de l'Université de Montréal (CHUM), Montreal, Quebec, Canada.
ORCID: 0000-0003-1955-9149

John G Lenehan (JG)

Department of Oncology, Western University, London, Ontario, Canada.
Lawson Health Research Institute, London, Ontario, Canada.

Wilson H Miller (WH)

Lady Davis Institute of the Jewish General Hospital, Segal Cancer Centre, Montreal, Quebec, Canada.
Departments of Oncology and Medicine, McGill University, Montreal, Quebec, Canada.

Rahima Jamal (R)

Research Center of the Centre Hospitalier de l'Université de Montréal, Montréal (CRCHUM), Montreal, Quebec, Canada.
Hematology-Oncology Division, Department of Medicine, Centre Hospitalier de l'Université de Montréal (CHUM), Montreal, Quebec, Canada.

Meriem Messaoudene (M)

Research Center of the Centre Hospitalier de l'Université de Montréal, Montréal (CRCHUM), Montreal, Quebec, Canada.

Brendan A Daisley (BA)

Department of Microbiology & Immunology, Western University, London, Ontario, Canada.
Canadian Centre for Human Microbiome and Probiotics Research, London, Ontario, Canada.
ORCID: 0000-0001-5999-5792

Cecilia Hes (C)

Research Center of the Centre Hospitalier de l'Université de Montréal, Montréal (CRCHUM), Montreal, Quebec, Canada.
Peter Brojde Lung Cancer Center, Jewish General Hospital, Montreal, Quebec, Canada.
ORCID: 0000-0002-4828-3260

Kait F Al (KF)

Lawson Health Research Institute, London, Ontario, Canada.
Department of Microbiology & Immunology, Western University, London, Ontario, Canada.
Canadian Centre for Human Microbiome and Probiotics Research, London, Ontario, Canada.
ORCID: 0000-0002-5905-6581

Laura Martinez-Gili (L)

Division of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, St Mary's Hospital Campus, Imperial College London, London, UK.
Section of Bioinformatics, Division of Systems Medicine, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UK.
ORCID: 0000-0001-5271-9672

Michal Punčochář (M)

Department of Computational, Cellular and Integrative Biology, University of Trento, Trento, Italy.
ORCID: 0000-0002-1915-9391

Scott Ernst (S)

Department of Oncology, Western University, London, Ontario, Canada.

Diane Logan (D)

Department of Oncology, Western University, London, Ontario, Canada.

Karl Belanger (K)

Research Center of the Centre Hospitalier de l'Université de Montréal, Montréal (CRCHUM), Montreal, Quebec, Canada.
Hematology-Oncology Division, Department of Medicine, Centre Hospitalier de l'Université de Montréal (CHUM), Montreal, Quebec, Canada.

Khashayar Esfahani (K)

Lady Davis Institute of the Jewish General Hospital, Segal Cancer Centre, Montreal, Quebec, Canada.
Departments of Oncology and Medicine, McGill University, Montreal, Quebec, Canada.

Corentin Richard (C)

Research Center of the Centre Hospitalier de l'Université de Montréal, Montréal (CRCHUM), Montreal, Quebec, Canada.

Marina Ninkov (M)

Department of Microbiology & Immunology, Western University, London, Ontario, Canada.

Gianmarco Piccinno (G)

Department of Computational, Cellular and Integrative Biology, University of Trento, Trento, Italy.

Federica Armanini (F)

Department of Computational, Cellular and Integrative Biology, University of Trento, Trento, Italy.

Federica Pinto (F)

Department of Computational, Cellular and Integrative Biology, University of Trento, Trento, Italy.
ORCID: 0000-0002-4539-4811

Mithunah Krishnamoorthy (M)

Department of Pathology and Laboratory Medicine, Western University, London, Ontario, Canada.

Rene Figueredo (R)

Department of Oncology, Western University, London, Ontario, Canada.

Pamela Thebault (P)

Research Center of the Centre Hospitalier de l'Université de Montréal, Montréal (CRCHUM), Montreal, Quebec, Canada.

Panteleimon Takis (P)

Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, National Phenome Centre, Imperial College London, London, UK.
Section of Bioanalytical Chemistry, Division of Systems Medicine, Department of Metabolism, Digestion and Reproduction, Imperial College London, London, UK.
ORCID: 0000-0002-7224-0412

Jamie Magrill (J)

Rosalind and Morris Goodman Cancer Institute, McGill University, Montréal, Quebec, Canada.

LeeAnn Ramsay (L)

Rosalind and Morris Goodman Cancer Institute, McGill University, Montréal, Quebec, Canada.

Lisa Derosa (L)

Gustave Roussy Cancer Campus, Villejuif, France.
Cancer Medicine Department, Gustave Roussy, Villejuif, France.
Institut National de la Santé Et et de la Recherche Médicale (INSERM) U1015, ClinicObiome, Equipe Labellisée-28 Ligue Nationale contre le Cancer, Villejuif, France.
Université Paris-Saclay, Ile-de-France, France.
ORCID: 0000-0003-0527-2964

Julian R Marchesi (JR)

Division of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, St Mary's Hospital Campus, Imperial College London, London, UK.

Seema Nair Parvathy (SN)

Department of Medicine, Division of Infectious Diseases, Western University, London, Ontario, Canada.
Division of Infectious Diseases, St Joseph's Health Care, London, Ontario, Canada.

Arielle Elkrief (A)

Research Center of the Centre Hospitalier de l'Université de Montréal, Montréal (CRCHUM), Montreal, Quebec, Canada.

Ian R Watson (IR)

Rosalind and Morris Goodman Cancer Institute, McGill University, Montréal, Quebec, Canada.
Department of Biochemistry, McGill University, Montréal, Quebec, Canada.
ORCID: 0000-0002-6025-3080

Rejean Lapointe (R)

Research Center of the Centre Hospitalier de l'Université de Montréal, Montréal (CRCHUM), Montreal, Quebec, Canada.
Département de Médecine, Faculté de Médecine, Université de Montréal, Montréal, Quebec, Canada.

Nicola Segata (N)

Department of Computational, Cellular and Integrative Biology, University of Trento, Trento, Italy.

S M Mansour Haeryfar (SMM)

Lawson Health Research Institute, London, Ontario, Canada.
Department of Microbiology & Immunology, Western University, London, Ontario, Canada.
Department of Medicine, Division of Clinical Immunology and Allergy, Western University, London, Ontario, Canada.
Department of Surgery, Division of General Surgery, Western University, London, Ontario, Canada.
ORCID: 0000-0002-1125-8176

Benjamin H Mullish (BH)

Division of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, St Mary's Hospital Campus, Imperial College London, London, UK.
Departments of Gastroenterology and Hepatology, St Mary's Hospital, Imperial College Healthcare NHS Trust, London, UK.
ORCID: 0000-0001-6300-3100

Michael S Silverman (MS)

Lawson Health Research Institute, London, Ontario, Canada.
Department of Microbiology & Immunology, Western University, London, Ontario, Canada.
Department of Medicine, Division of Infectious Diseases, Western University, London, Ontario, Canada.
Division of Infectious Diseases, St Joseph's Health Care, London, Ontario, Canada.

Jeremy P Burton (JP)

Lawson Health Research Institute, London, Ontario, Canada.
Department of Microbiology & Immunology, Western University, London, Ontario, Canada.
Canadian Centre for Human Microbiome and Probiotics Research, London, Ontario, Canada.
ORCID: 0000-0002-3591-6436

Saman Maleki Vareki (S)

Department of Oncology, Western University, London, Ontario, Canada. saman.malekivareki@lhsc.on.ca.
Lawson Health Research Institute, London, Ontario, Canada. saman.malekivareki@lhsc.on.ca.
Department of Pathology and Laboratory Medicine, Western University, London, Ontario, Canada. saman.malekivareki@lhsc.on.ca.
Department of Medical Biophysics, Western University, London, Ontario, Canada. saman.malekivareki@lhsc.on.ca.
Ontario Institute of Cancer Research, Toronto, Ontario, Canada. saman.malekivareki@lhsc.on.ca.
ORCID: 0000-0002-9615-7779

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