Gut Microbiota Dynamics during Chemotherapy in Epithelial Ovarian Cancer Patients Are Related to Therapeutic Outcome

Epithelial ovarian cancer (EOC) is one of the most lethal and silent gynecological tumors. Despite appropriate surgery and chemotherapy, relapse occurs in over half of patients with a poor prognosis. Recently, the gut microbiota (GM) was hypothesized to influence the efficacy of anticancer therapies...

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Published inCancers Vol. 13; no. 16; p. 3999
Main Authors D’Amico, Federica, Perrone, Anna Myriam, Rampelli, Simone, Coluccelli, Sara, Barone, Monica, Ravegnini, Gloria, Fabbrini, Marco, Brigidi, Patrizia, De Iaco, Pierandrea, Turroni, Silvia
Format Journal Article
LanguageEnglish
Published Basel MDPI AG 08.08.2021
MDPI
Subjects
Animal models
Cancer therapies
Chemotherapy
Feces
Gene amplification
Gynecology
Human papillomavirus
Intestinal microflora
Lactic acid
Medical prognosis
Metagenomics
Microbiota
Microorganisms
Ovarian cancer
Pathogenesis
Patients
Platinum
Prognosis
rRNA 16S
Tumors
United States > US
Italy
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Abstract Epithelial ovarian cancer (EOC) is one of the most lethal and silent gynecological tumors. Despite appropriate surgery and chemotherapy, relapse occurs in over half of patients with a poor prognosis. Recently, the gut microbiota (GM) was hypothesized to influence the efficacy of anticancer therapies, but no data are available in EOC. Here, by 16S rRNA gene sequencing and inferred metagenomics, we profiled the GM of EOC patients at diagnosis and reconstructed its trajectory along the course of neoadjuvant or adjuvant chemotherapy up to follow-up. Compared to healthy subjects, the GM of EOC patients appeared unbalanced and severely affected by chemotherapy. Strikingly, discriminating patterns were identified in relation to the therapeutic response. Platinum-resistant patients showed a marked temporal reduction in GM diversity and increased instability with loss of health-associated taxa and increased proportions of Coriobacteriaceae and Bifidobacterium. Notably, most of these microorganisms are lactate producers, suggesting increased lactate production as supported by inferred metagenomics. In contrast, the GM of platinum-sensitive patients appeared overall more diverse and stable and enriched in lactate utilizers from the Veillonellaceae family. In conclusion, we identified potential GM signatures of therapeutic outcome in EOC patients, which could open up new opportunities for cancer prognosis and treatment.
AbstractList Epithelial ovarian cancer (EOC) is one of the most lethal and silent gynecological tumors. Despite appropriate surgery and chemotherapy, relapse occurs in over half of patients with a poor prognosis. Recently, the gut microbiota (GM) was hypothesized to influence the efficacy of anticancer therapies, but no data are available in EOC. Here, by 16S rRNA gene sequencing and inferred metagenomics, we profiled the GM of EOC patients at diagnosis and reconstructed its trajectory along the course of neoadjuvant or adjuvant chemotherapy up to follow-up. Compared to healthy subjects, the GM of EOC patients appeared unbalanced and severely affected by chemotherapy. Strikingly, discriminating patterns were identified in relation to the therapeutic response. Platinum-resistant patients showed a marked temporal reduction in GM diversity and increased instability with loss of health-associated taxa and increased proportions of Coriobacteriaceae and Bifidobacterium. Notably, most of these microorganisms are lactate producers, suggesting increased lactate production as supported by inferred metagenomics. In contrast, the GM of platinum-sensitive patients appeared overall more diverse and stable and enriched in lactate utilizers from the Veillonellaceae family. In conclusion, we identified potential GM signatures of therapeutic outcome in EOC patients, which could open up new opportunities for cancer prognosis and treatment.
Simple SummaryThis pilot study on the trajectory of the gut microbiota (GM) in patients with epithelial ovarian cancer undergoing neoadjuvant and adjuvant chemotherapy highlighted peculiar dynamics associated with the therapeutic outcome. In particular, platinum-resistant patients showed a marked temporal reduction in GM diversity and increased instability with loss of health-associated taxa and increased proportions of lactate-producing microorganisms compared to those sensitive to platinum. These potential GM signatures of therapeutic failure are detectable within the first half of chemotherapy cycles, suggesting that early integrated treatments also aimed at modulating GM could influence therapeutic outcome. Further studies in larger cohorts combining multiple omics and possibly animal models are urgently needed for in-depth mechanistic understanding.AbstractEpithelial ovarian cancer (EOC) is one of the most lethal and silent gynecological tumors. Despite appropriate surgery and chemotherapy, relapse occurs in over half of patients with a poor prognosis. Recently, the gut microbiota (GM) was hypothesized to influence the efficacy of anticancer therapies, but no data are available in EOC. Here, by 16S rRNA gene sequencing and inferred metagenomics, we profiled the GM of EOC patients at diagnosis and reconstructed its trajectory along the course of neoadjuvant or adjuvant chemotherapy up to follow-up. Compared to healthy subjects, the GM of EOC patients appeared unbalanced and severely affected by chemotherapy. Strikingly, discriminating patterns were identified in relation to the therapeutic response. Platinum-resistant patients showed a marked temporal reduction in GM diversity and increased instability with loss of health-associated taxa and increased proportions of Coriobacteriaceae and Bifidobacterium. Notably, most of these microorganisms are lactate producers, suggesting increased lactate production as supported by inferred metagenomics. In contrast, the GM of platinum-sensitive patients appeared overall more diverse and stable and enriched in lactate utilizers from the Veillonellaceae family. In conclusion, we identified potential GM signatures of therapeutic outcome in EOC patients, which could open up new opportunities for cancer prognosis and treatment.
Epithelial ovarian cancer (EOC) is one of the most lethal and silent gynecological tumors. Despite appropriate surgery and chemotherapy, relapse occurs in over half of patients with a poor prognosis. Recently, the gut microbiota (GM) was hypothesized to influence the efficacy of anticancer therapies, but no data are available in EOC. Here, by 16S rRNA gene sequencing and inferred metagenomics, we profiled the GM of EOC patients at diagnosis and reconstructed its trajectory along the course of neoadjuvant or adjuvant chemotherapy up to follow-up. Compared to healthy subjects, the GM of EOC patients appeared unbalanced and severely affected by chemotherapy. Strikingly, discriminating patterns were identified in relation to the therapeutic response. Platinum-resistant patients showed a marked temporal reduction in GM diversity and increased instability with loss of health-associated taxa and increased proportions of Coriobacteriaceae and Bifidobacterium. Notably, most of these microorganisms are lactate producers, suggesting increased lactate production as supported by inferred metagenomics. In contrast, the GM of platinum-sensitive patients appeared overall more diverse and stable and enriched in lactate utilizers from the Veillonellaceae family. In conclusion, we identified potential GM signatures of therapeutic outcome in EOC patients, which could open up new opportunities for cancer prognosis and treatment.Epithelial ovarian cancer (EOC) is one of the most lethal and silent gynecological tumors. Despite appropriate surgery and chemotherapy, relapse occurs in over half of patients with a poor prognosis. Recently, the gut microbiota (GM) was hypothesized to influence the efficacy of anticancer therapies, but no data are available in EOC. Here, by 16S rRNA gene sequencing and inferred metagenomics, we profiled the GM of EOC patients at diagnosis and reconstructed its trajectory along the course of neoadjuvant or adjuvant chemotherapy up to follow-up. Compared to healthy subjects, the GM of EOC patients appeared unbalanced and severely affected by chemotherapy. Strikingly, discriminating patterns were identified in relation to the therapeutic response. Platinum-resistant patients showed a marked temporal reduction in GM diversity and increased instability with loss of health-associated taxa and increased proportions of Coriobacteriaceae and Bifidobacterium. Notably, most of these microorganisms are lactate producers, suggesting increased lactate production as supported by inferred metagenomics. In contrast, the GM of platinum-sensitive patients appeared overall more diverse and stable and enriched in lactate utilizers from the Veillonellaceae family. In conclusion, we identified potential GM signatures of therapeutic outcome in EOC patients, which could open up new opportunities for cancer prognosis and treatment.
Author Brigidi, Patrizia
De Iaco, Pierandrea
Barone, Monica
Coluccelli, Sara
Ravegnini, Gloria
Perrone, Anna Myriam
Turroni, Silvia
D’Amico, Federica
Rampelli, Simone
Fabbrini, Marco
AuthorAffiliation 3 Division of Oncologic Gynecology, IRCCS Azienda Ospedaliero, University of Bologna, 40138 Bologna, Italy
4 Centro di Studio e Ricerca delle Neoplasie Ginecologiche (CSR), University of Bologna, 40138 Bologna, Italy
1 Department of Medical and Surgical Sciences, University of Bologna, 40138 Bologna, Italy; myriam.perrone@aosp.bo.it (A.M.P.); sara.coluccelli2@unibo.it (S.C.); monica.barone@unibo.it (M.B.); patrizia.brigidi@unibo.it (P.B.); pierandrea.deiaco@unibo.it (P.D.I.)
2 Department of Pharmacy and Biotechnology, University of Bologna, 40126 Bologna, Italy; simone.rampelli@unibo.it (S.R.); gloria.ravegnini2@unibo.it (G.R.); m.fabbrini@unibo.it (M.F.); silvia.turroni@unibo.it (S.T.)
AuthorAffiliation_xml – name: 3 Division of Oncologic Gynecology, IRCCS Azienda Ospedaliero, University of Bologna, 40138 Bologna, Italy
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– name: 4 Centro di Studio e Ricerca delle Neoplasie Ginecologiche (CSR), University of Bologna, 40138 Bologna, Italy
– name: 2 Department of Pharmacy and Biotechnology, University of Bologna, 40126 Bologna, Italy; simone.rampelli@unibo.it (S.R.); gloria.ravegnini2@unibo.it (G.R.); m.fabbrini@unibo.it (M.F.); silvia.turroni@unibo.it (S.T.)
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Snippet Epithelial ovarian cancer (EOC) is one of the most lethal and silent gynecological tumors. Despite appropriate surgery and chemotherapy, relapse occurs in over...
Simple SummaryThis pilot study on the trajectory of the gut microbiota (GM) in patients with epithelial ovarian cancer undergoing neoadjuvant and adjuvant...
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StartPage 3999
SubjectTerms Animal models
Cancer therapies
Chemotherapy
Feces
Gene amplification
Gynecology
Human papillomavirus
Intestinal microflora
Lactic acid
Medical prognosis
Metagenomics
Microbiota
Microorganisms
Ovarian cancer
Pathogenesis
Patients
Platinum
Prognosis
rRNA 16S
Tumors
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Title Gut Microbiota Dynamics during Chemotherapy in Epithelial Ovarian Cancer Patients Are Related to Therapeutic Outcome
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https://pubmed.ncbi.nlm.nih.gov/PMC8393652
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