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Cross-cohort gut microbiome associations with immune checkpoint inhibitor response in advanced melanoma
Karla A. Lee (King's College London), Andrew Maltez Thomas (University of Trento), Laura A. Bolte (University Medical Center Groningen, University of Groningen), Johannes R. Björk (University Medical Center Groningen, University of Groningen), Laura Kist de Ruijter (University Medical Center Groningen, University of Groningen), Federica Armanini (University of Trento), Francesco Asnicar (University of Trento), Aitor Blanco‐Míguez (University of Trento), Ruth Board (Lancashire Teaching Hospitals NHS Foundation Trust), Neus Calbet‐Llopart (Instituto de Salud Carlos III, Hospital Clínic de Barcelona), Lisa Derosa (Inserm, Université Paris-Saclay), Nathalie S. Dhomen (University of Manchester, Cancer Research UK Manchester Institute), Kelly M. Brooks (University of Manchester, Cancer Research UK Manchester Institute), Mark Harland (University of Leeds), Mark Harries (Guy's Hospital, Guy's and St Thomas' NHS Foundation Trust), Emily R. Leeming (King's College London), Paul C. Lorigan (University of Manchester, The Christie NHS Foundation Trust), Paolo Manghi (University of Trento), Richard Marais (University of Manchester, Cancer Research UK Manchester Institute), Julia Newton‐Bishop (University of Leeds), Luigi Nezi (European Institute of Oncology), Federica Pinto (University of Trento), Míriam Potrony (Instituto de Salud Carlos III, Hospital Clínic de Barcelona), Susana Puig (Instituto de Salud Carlos III, Hospital Clínic de Barcelona), Patricio Serra-Bellver (The Christie NHS Foundation Trust), Heather May Shaw (Mount Vernon Cancer Centre), Sabrina Tamburini (European Institute of Oncology), Sara Valpione (University of Manchester, Cancer Research UK Manchester Institute), Amrita Vijay (University of Nottingham, King's College London), Levi Waldron (City University of New York, University of Trento), Laurence Zitvogel (Inserm, Université Paris-Saclay), Moreno Zolfo (University of Trento), Elisabeth G.E. de Vries (University Medical Center Groningen, University of Groningen), Paul Nathan (Hospital Clínic de Barcelona, Consorci Institut D'Investigacions Biomediques August Pi I Sunyer), Rudolf S.N. Fehrmann (University Medical Center Groningen, University of Groningen), Veronique A. Bataille (King's College London, Mount Vernon Cancer Centre), Geke A.P. Hospers (University Medical Center Groningen, University of Groningen), Tim D. Spector (King's College London), Rinse Karel Weersma (University Medical Center Groningen, University of Groningen), Nicola Segata (University of Trento, European Institute of Oncology)
Abstract: The composition of the gut microbiome has been associated with clinical responses to immune checkpoint inhibitor (ICI) treatment, but there is limited consensus on the specific microbiome characteristics linked to the clinical benefits of ICIs. We performed shotgun metagenomic sequencing of stool samples collected before ICI initiation from five observational cohorts recruiting ICI-naive patients with advanced cutaneous melanoma (n = 165). Integrating the dataset with 147 metagenomic samples from previously published studies, we found that the gut microbiome has a relevant, but cohort-dependent, association with the response to ICIs. A machine learning analysis confirmed the link between the microbiome and overall response rates (ORRs) and progression-free survival (PFS) with ICIs but also revealed limited reproducibility of microbiome-based signatures across cohorts. Accordingly, a panel of species, including Bifidobacterium pseudocatenulatum, Roseburia spp. and Akkermansia muciniphila, associated with responders was identified, but no single species could be regarded as a fully consistent biomarker across studies. Overall, the role of the human gut microbiome in ICI response appears more complex than previously thought, extending beyond differing microbial species simply present or absent in responders and nonresponders. Future studies should adopt larger sample sizes and take into account the complex interplay of clinical factors with the gut microbiome over the treatment course.