Intratumoral microbiota composition in women’s cancers: a systematic review and meta-analysis
BackgroundThe intratumoral microbiota has attracted considerable interest in carcinogenesis, progression, and treatment owing to advancements in sequencing technology. This systematic review provides a comprehensive overview of the current literature regarding the diversity and compositional charact...
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Frontiers Media S.A.
2025-06-01
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| Series: | Frontiers in Oncology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fonc.2025.1544786/full |
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| author | Qin Wen Qin Wen Shubin Wang Shubin Wang Shunlian Fu Xinxiang Zhou Xinxiang Zhou Yalan Min Yalan Min Jinyi Lang Jinyi Lang Meihua Chen |
| author_facet | Qin Wen Qin Wen Shubin Wang Shubin Wang Shunlian Fu Xinxiang Zhou Xinxiang Zhou Yalan Min Yalan Min Jinyi Lang Jinyi Lang Meihua Chen |
| author_sort | Qin Wen |
| collection | DOAJ |
| description | BackgroundThe intratumoral microbiota has attracted considerable interest in carcinogenesis, progression, and treatment owing to advancements in sequencing technology. This systematic review provides a comprehensive overview of the current literature regarding the diversity and compositional characteristics of the intratumoral microbiota in women’s cancers. Additionally, it also explores potential associations among intratumoral microbiota, estrogen, and anti-tumor therapies.MethodsA comprehensive literature search was conducted using PubMed, Embase, Web of Science, and the Cochrane Library from their inception to May 1, 2024. The review protocol was pre-registered in PROSPERO (CRD 42024601213). Articles were assessed utilizing the Newcastle-Ottawa Scale (NOS). To estimate the effect size and variability in microbial diversity changes, the standardized mean difference (SMD) and 95% confidence intervals (CIs) were employed. The systematic review adhered to PRISMA reporting guidelines, and meta-analyses were performed using Review Manager version 5.4.ResultsThis systematic review included 29 of 8,291 studies after a thorough screening process. Of the 22 studies investigating α-diversity in women’s cancers, disease-free controls, and those with benign conditions, notable changes in diversity indices were observed. Compared to adjacent normal tissues, the Simpson index significantly decreased in breast cancer (SMD = -0.75, 95% CI: [-0.94, -0.55]) and endometrial cancer (SMD = -0.83, 95% CI: [-1.37, -0.28]). The Chao1 index was reduced in endometrial cancer tumor tissues relative to normal tissues (SMD = -2.25, 95% CI: [-3.13, -1.36]), while the Shannon index decreased in ovarian cancer tumor tissues (SMD = -0.61, 95% CI: [-1.18, -0.04]). In comparisons between tumor and benign tissues, the Chao1 index was decreased (SMD = -0.64, 95% CI: [-1.20, -0.08], I² = 0%), while the Simpson index was increased (SMD = 0.36, 95% CI: [0.01, 0.71], I² = 0%) in patients with ovarian cancer. Other microbial diversity indices showed no significant differences between tumor and non-tumor tissues. At the phylum level, Fusobacteriota were enriched in tumor tissues, while Firmicutes and Actinobacteria predominated in non-tumor tissues. At the genus level, Pseudomonas, Porphyromonas, Atopobium, Peptoniphilus, and Acinetobacter were consistently more abundant in cancerous tissues. Microbial alterations were also linked to estrogen receptor (ER) status, with Alkanindiges negatively correlated with ER status in two studies. Furthermore, one study on the effect of antineoplastic therapy indicated that neoadjuvant chemotherapy reduced microbial diversity in breast cancer patients (n = 15 vs. n = 18) (Shannon index: SMD = -0.95, 95% CI: [-1.68, -0.22]).ConclusionThis study highlights significant differences in microbiota composition between tumor and non-tumor tissues in women’s cancers, emphasizing changes in intratumoral microbiota influenced by estrogen and antineoplastic treatments. Further research is needed to explore the potential for developing targeted therapies based on estrogen-driven microbiota alterations. Investigations may yield insights into the enhancement of female reproductive health and the improvement of treatment efficacy for female cancers.Systematic review registrationhttps://www.crd.york.ac.uk/PROSPERO/view/CRD42024601213, identifier CRD 42024601213. |
| format | Article |
| id | doaj-art-014ed74bdf0a495ab0b439a79ba7c774 |
| institution | OA Journals |
| issn | 2234-943X |
| language | English |
| publishDate | 2025-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Oncology |
| spelling | doaj-art-014ed74bdf0a495ab0b439a79ba7c7742025-08-20T02:23:05ZengFrontiers Media S.A.Frontiers in Oncology2234-943X2025-06-011510.3389/fonc.2025.15447861544786Intratumoral microbiota composition in women’s cancers: a systematic review and meta-analysisQin Wen0Qin Wen1Shubin Wang2Shubin Wang3Shunlian Fu4Xinxiang Zhou5Xinxiang Zhou6Yalan Min7Yalan Min8Jinyi Lang9Jinyi Lang10Meihua Chen11School of Medicine, University of Electronic Science and Technology of China, Chengdu, ChinaDepartment of Radiation Oncology, Radiation Oncology Key Laboratory of Sichuan Province, Sichuan Clinical Research Center for Cancer, Sichuan Cancer Center, Sichuan Cancer Hospital & Institute, Affiliated Cancer Hospital of University of Electronic Science and Technology of China, Chengdu, ChinaSchool of Medicine, University of Electronic Science and Technology of China, Chengdu, ChinaDepartment of Radiation Oncology, Radiation Oncology Key Laboratory of Sichuan Province, Sichuan Clinical Research Center for Cancer, Sichuan Cancer Center, Sichuan Cancer Hospital & Institute, Affiliated Cancer Hospital of University of Electronic Science and Technology of China, Chengdu, ChinaSchool of Clinical Medicine, Chengdu University of Traditional Chinese Medicine, Chengdu, ChinaSchool of Medicine, University of Electronic Science and Technology of China, Chengdu, ChinaDepartment of Radiation Oncology, Radiation Oncology Key Laboratory of Sichuan Province, Sichuan Clinical Research Center for Cancer, Sichuan Cancer Center, Sichuan Cancer Hospital & Institute, Affiliated Cancer Hospital of University of Electronic Science and Technology of China, Chengdu, ChinaSchool of Medicine, University of Electronic Science and Technology of China, Chengdu, ChinaDepartment of Radiation Oncology, Radiation Oncology Key Laboratory of Sichuan Province, Sichuan Clinical Research Center for Cancer, Sichuan Cancer Center, Sichuan Cancer Hospital & Institute, Affiliated Cancer Hospital of University of Electronic Science and Technology of China, Chengdu, ChinaSchool of Medicine, University of Electronic Science and Technology of China, Chengdu, ChinaDepartment of Radiation Oncology, Radiation Oncology Key Laboratory of Sichuan Province, Sichuan Clinical Research Center for Cancer, Sichuan Cancer Center, Sichuan Cancer Hospital & Institute, Affiliated Cancer Hospital of University of Electronic Science and Technology of China, Chengdu, ChinaDepartment of Radiation Oncology, Radiation Oncology Key Laboratory of Sichuan Province, Sichuan Clinical Research Center for Cancer, Sichuan Cancer Center, Sichuan Cancer Hospital & Institute, Affiliated Cancer Hospital of University of Electronic Science and Technology of China, Chengdu, ChinaBackgroundThe intratumoral microbiota has attracted considerable interest in carcinogenesis, progression, and treatment owing to advancements in sequencing technology. This systematic review provides a comprehensive overview of the current literature regarding the diversity and compositional characteristics of the intratumoral microbiota in women’s cancers. Additionally, it also explores potential associations among intratumoral microbiota, estrogen, and anti-tumor therapies.MethodsA comprehensive literature search was conducted using PubMed, Embase, Web of Science, and the Cochrane Library from their inception to May 1, 2024. The review protocol was pre-registered in PROSPERO (CRD 42024601213). Articles were assessed utilizing the Newcastle-Ottawa Scale (NOS). To estimate the effect size and variability in microbial diversity changes, the standardized mean difference (SMD) and 95% confidence intervals (CIs) were employed. The systematic review adhered to PRISMA reporting guidelines, and meta-analyses were performed using Review Manager version 5.4.ResultsThis systematic review included 29 of 8,291 studies after a thorough screening process. Of the 22 studies investigating α-diversity in women’s cancers, disease-free controls, and those with benign conditions, notable changes in diversity indices were observed. Compared to adjacent normal tissues, the Simpson index significantly decreased in breast cancer (SMD = -0.75, 95% CI: [-0.94, -0.55]) and endometrial cancer (SMD = -0.83, 95% CI: [-1.37, -0.28]). The Chao1 index was reduced in endometrial cancer tumor tissues relative to normal tissues (SMD = -2.25, 95% CI: [-3.13, -1.36]), while the Shannon index decreased in ovarian cancer tumor tissues (SMD = -0.61, 95% CI: [-1.18, -0.04]). In comparisons between tumor and benign tissues, the Chao1 index was decreased (SMD = -0.64, 95% CI: [-1.20, -0.08], I² = 0%), while the Simpson index was increased (SMD = 0.36, 95% CI: [0.01, 0.71], I² = 0%) in patients with ovarian cancer. Other microbial diversity indices showed no significant differences between tumor and non-tumor tissues. At the phylum level, Fusobacteriota were enriched in tumor tissues, while Firmicutes and Actinobacteria predominated in non-tumor tissues. At the genus level, Pseudomonas, Porphyromonas, Atopobium, Peptoniphilus, and Acinetobacter were consistently more abundant in cancerous tissues. Microbial alterations were also linked to estrogen receptor (ER) status, with Alkanindiges negatively correlated with ER status in two studies. Furthermore, one study on the effect of antineoplastic therapy indicated that neoadjuvant chemotherapy reduced microbial diversity in breast cancer patients (n = 15 vs. n = 18) (Shannon index: SMD = -0.95, 95% CI: [-1.68, -0.22]).ConclusionThis study highlights significant differences in microbiota composition between tumor and non-tumor tissues in women’s cancers, emphasizing changes in intratumoral microbiota influenced by estrogen and antineoplastic treatments. Further research is needed to explore the potential for developing targeted therapies based on estrogen-driven microbiota alterations. Investigations may yield insights into the enhancement of female reproductive health and the improvement of treatment efficacy for female cancers.Systematic review registrationhttps://www.crd.york.ac.uk/PROSPERO/view/CRD42024601213, identifier CRD 42024601213.https://www.frontiersin.org/articles/10.3389/fonc.2025.1544786/fullintratumoral microbiota16s rrna gene sequencingbreast cancergynecologic cancerestrogenmeta-analysis |
| spellingShingle | Qin Wen Qin Wen Shubin Wang Shubin Wang Shunlian Fu Xinxiang Zhou Xinxiang Zhou Yalan Min Yalan Min Jinyi Lang Jinyi Lang Meihua Chen Intratumoral microbiota composition in women’s cancers: a systematic review and meta-analysis Frontiers in Oncology intratumoral microbiota 16s rrna gene sequencing breast cancer gynecologic cancer estrogen meta-analysis |
| title | Intratumoral microbiota composition in women’s cancers: a systematic review and meta-analysis |
| title_full | Intratumoral microbiota composition in women’s cancers: a systematic review and meta-analysis |
| title_fullStr | Intratumoral microbiota composition in women’s cancers: a systematic review and meta-analysis |
| title_full_unstemmed | Intratumoral microbiota composition in women’s cancers: a systematic review and meta-analysis |
| title_short | Intratumoral microbiota composition in women’s cancers: a systematic review and meta-analysis |
| title_sort | intratumoral microbiota composition in women s cancers a systematic review and meta analysis |
| topic | intratumoral microbiota 16s rrna gene sequencing breast cancer gynecologic cancer estrogen meta-analysis |
| url | https://www.frontiersin.org/articles/10.3389/fonc.2025.1544786/full |
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