Microbial Omens: The Predictive Power of Microbiome Signatures in Cancer Risk
DOI:
https://doi.org/10.15407/microbiolj87.03.099Keywords:
microbiome, prediction, cancer, diagnosisAbstract
The human microbiome, a complex ecosystem of microorganisms inhabiting various niches within the body, has emerged as a potential harbinger of health and disease. In recent years, a growing body of research has illuminated the intricate interplay between the microbiome and cancer risk. This review article explores the burgeoning field of microbiome signatures as predictive tools for assessing the risk of cancer development. The microbiome's role in maintaining homeostasis, modulating immune responses, and influencing metabolic pathways has provided a fertile ground for investigating its association with carcinogenesis. With a focus on distinct microbial compositions and specific molecular markers, we delve into the intricate mechanisms underlying the potential of microbiome signatures to forecast cancer risk. From gastrointestinal to genitourinary malignancies, we survey the landscape of microbiome-related studies that have unveiled promising associations between microbial dysbiosis and the initiation of carcinogenesis. Furthermore, we discuss the integration of cutting-edge technologies, including high-throughput sequencing and advanced bioinformatics, in deciphering complex microbiome data and deriving predictive models. The challenges of standardization, validation, and clinical translation of microbiome-based risk assessments are also addressed. As microbiome research evolves, it offers unprecedented insights into the early stages of cancer development, heralding a paradigm shift in personalized cancer risk assessment. By presenting an overview of current achievements, limitations, and prospects, this review elucidates the transformative potential of microbial omens in shaping the landscape of cancer prediction and preventive strategies.
Downloads
References
Anipindi, M., & Bitetto, D. (2022). Diagnostic and Therapeutic Uses of the Microbiome in the Field of Oncology. Cureus, 14(5). https://doi.org/10.7759/cureus.24890
Arthur, J. C., Perez-Chanona, E., Mühlbauer, M., Tomkovich, S., Uronis, J. M., Fan, T.-J., Campbell, B. J., Abujamel, T., Dogan, B., Rogers, A. B., Rhodes, J. M., Stintzi, A., Simpson, K. W., Hansen, J. J., Keku, T. O., Fodor, A. A., & Jobin, C. (2012). Intestinal Inflammation Targets Cancer-Inducing Activity of the Microbiota. Science, 338(6103), 120-123. https://doi.org/10.1126/science.1224820
Bajic, P., Wolfe, A. J., & Gupta, G. N. (2019). The Urinary Microbiome: Implications in Bladder Cancer Pathogenesis and Therapeutics. Urology, 126, 10-15. https://doi.org/10.1016/j.urology.2018.12.034
Balkwill, F., & Mantovani, A. (2001). Inflammation and cancer: back to Virchow? The Lancet, 357(9255), 539-545. https://doi.org/10.1016/S0140-6736(00)04046-0
Banerjee, S., Tian, T., Wei, Z., Shih, N., Feldman, M. D., Alwine, J. C., Coukos, G., & Robertson, E. S. (2017). The ovarian cancer oncobiome. Oncotarget, 8(22), 36225-36245. https://doi.org/10.18632/oncotarget.16717
Belkaid, Y., & Hand, Timothy W. (2014). Role of the Microbiota in Immunity and Inflammation. Cell, 157(1), 121-141. https://doi.org/10.1016/j.cell.2014.03.011
Binder Gallimidi, A., Fischman, S., Revach, B., Bulvik, R., Maliutina, A., Rubinstein, A. M., Nussbaum, G., & Elkin, M. (2015). Periodontal pathogens Porphyromonas gingivalis and Fusobacterium nucleatum promote tumor progression in an oral-specific chemical carcinogenesis model. Oncotarget, 6(26), 22613-22623. https://doi.org/10.18632/oncotarget.4209
Börnigen, D., Ren, B., Pickard, R., Li, J., Ozer, E., Hartmann, E. M., Xiao, W., Tickle, T., Rider, J., Gevers, D., Franzosa, E. A., Davey, M. E., Gillison, M. L., & Huttenhower, C. (2017). Alterations in oral bacterial communities are associated with risk factors for oral and oropharyngeal cancer. Scientific Reports, 7(1). https://doi.org/10.1038/s41598-017-17795-z
Canani, R. B. (2011). Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World Journal of Gastroenterology, 17(12), 1519. https://doi.org/10.3748/wjg.v17.i12.1519
Cani, P. D., Bibiloni, R., Knauf, C., Waget, A., Neyrinck, A. M., Delzenne, N. M., & Burcelin, R. (2008). Changes in Gut Microbiota Control Metabolic Endotoxemia-Induced Inflammation in High-Fat Diet-Induced Obesity and Diabetes in Mice. Diabetes, 57(6), 1470-1481. https://doi.org/10.2337/db07-1403
Davie, J. R. (2003). Inhibition of Histone Deacetylase Activity by Butyrate. The Journal of Nutrition, 133(7), 2485S2493S. https://doi.org/10.1093/jn/133.7.2485S
dos Reis, S. A., da Conceição, L. L., & Peluzio, M. do C. G. (2019). Intestinal microbiota and colorectal cancer: changes in the intestinal microenvironment and their relation to the disease. Journal of Medical Microbiology, 68(10), 1391-1407. https://doi.org/10.1099/jmm.0.001049
Fakruddin, Md., Md. Asaduzzaman Shishir, Israk Iram Oyshe, Amin, T., Hossain, A., Israt Jahan Sarna, Jerin, N., & Dipak Kumar Mitra. (2023). Microbial Architects of Malignancy: Exploring the Gut Microbiome's Influence in Cancer Initiation and Progression. Cancer Plus, 5(1), 1. https://doi.org/10.18063/cp.397
Farrell, J. J., Zhang, L., Zhou, H., Chia, D., Elashoff, D., Akin, D., Paster, B. J., Joshipura, K., & Wong, D. T. W. (2012). Variations of oral microbiota are associated with pancreatic diseases including pancreatic cancer. Gut, 61(4), 582-588. https://doi.org/10.1136/gutjnl-2011-300784
Furusawa, Y., Obata, Y., Fukuda, S., Endo, T. A., Nakato, G., Takahashi, D., Nakanishi, Y., Uetake, C., Kato, K., Kato, T., Takahashi, M., Fukuda, N. N., Murakami, S., Miyauchi, E., Hino, S., Atarashi, K., Onawa, S., Fujimura, Y., Lockett, T., & Clarke, J. M. (2013). Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature, 504(7480), 446-450. https://doi.org/10.1038/nature12721
Garrett, W. S. (2015). Cancer and the microbiota. Science (New York, N.Y.), 348(6230), 80-86. https://doi.org/10.1126/science.aaa4972
Guerrero-Preston, R., Godoy-Vitorino, F., Jedlicka, A., Rodríguez-Hilario, A., González, H., Bondy, J., Lawson, F., Folawiyo, O., Michailidi, C., Dziedzic, A., Thangavel, R., Hadar, T., Noordhuis, M. G., Westra, W., Koch, W., & Sidransky, D. (2016). 16S rRNA amplicon sequencing identifies microbiota associated with oral cancer, human papilloma virus infection and surgical treatment. Oncotarget, 7(32), 51320-51334. https://doi.org/10.18632/oncotarget.9710
Guertin, K. A., Li, X. S., Graubard, B. I., Albanes, D., Weinstein, S. J., Goedert, J. J., Wang, Z., Hazen, S. L., & Sinha, R. (2017). Serum Trimethylamine N-oxide, Carnitine, Choline, and Betaine in Relation to Colorectal Cancer Risk in the Alpha Tocopherol, Beta Carotene Cancer Prevention Study. Cancer Epidemiology, Biomarkers & Prevention, 26(6), 945-952. https://doi.org/10.1158/1055-9965.EPI-16-0948
Hanahan, D. (2022). Hallmarks of Cancer: New Dimensions. Cancer Discovery, 12(1), 31-46. https://doi.org/10.1158/2159-8290.CD-21-1059
Hermida, L. C., Gertz, E. M., & Ruppin, E. (2022). Predicting cancer prognosis and drug response from the tumor microbiome. Nature Communications, 13(1), 2896. https://doi.org/10.1038/s41467-022-30512-3
Hosgood, H. D., Sapkota, A. R., Rothman, N., Rohan, T., Hu, W., Xu, J., Vermeulen, R., He, X., White, J. R., Wu, G., Wei, F., Mongodin, E. F., & Lan, Q. (2014). The potential role of lung microbiota in lung cancer attributed to household coal burning exposures. Environmental and Molecular Mutagenesis, 55(8), 643-651. https://doi.org/10.1002/em.21878
Huang, J., & Huang, J. (2022). Microbial Biomarkers for Lung Cancer: Current Understandings and Limitations. Journal of Clinical Medicine, 11(24), 7298. https://doi.org/10.3390/jcm11247298
Ishaq, S., & Nunn, L. (2015). Helicobacter pylori and gastric cancer: a state of the art review. Gastroenterology and Hepatology from Bed to Bench, 8(Suppl 1), S6-S14.
Jarman, R., Ribeiro-Milograna, S., & Kalle, W. (2020). Potential of the Microbiome as a Biomarker for Early Diagnosis and Prognosis of Breast Cancer. Journal of Breast Cancer, 23(6). https://doi.org/10.4048/jbc.2020.23.e60
Jin, C., Lagoudas, G. K., Zhao, C., Bullman, S., Bhutkar, A., Hu, B., Ameh, S., Sandel, D., Liang, X. S., Mazzilli, S., Whary, M. T., Meyerson, M., Germain, R., Blainey, P. C., Fox, J. G., & Jacks, T. (2019). Commensal Microbiota Promote Lung Cancer Development via γδ T Cells. Cell, 176(5), 998-1013.e16. https://doi.org/10.1016/j.cell.2018.12.040
Kandalai, S., Li, H., Zhang, N., Peng, H., & Zheng, Q. (2023). The human microbiome and cancer: a diagnostic and therapeutic perspective. Cancer Biology & Therapy, 24(1). https://doi.org/10.1080/15384047.2023.2240084
Kartal, E., Schmidt, T. S. B., Molina-Montes, E., Rodríguez-Perales, S., Wirbel, J., Maistrenko, O. M., Akanni, W. A., Alashkar Alhamwe, B., Alves, R. J., Carrato, A., Erasmus, H.-P., Estudillo, L., Finkelmeier, F., Fullam, A., Glazek, A. M., Gómez-Rubio, P., Hercog, R., Jung, F., Kandels, S., & Kersting, S. (2022). A faecal microbiota signature with high specificity for pancreatic cancer. Gut, gutjnl-2021-324755. https://doi.org/10.1136/gutjnl-2021-324755
Krigul, K. L., Aasmets, O., Kreete Lüll, Tõnis Org, & Org, E. (2021). Using fecal immunochemical tubes for the analysis of the gut microbiome has the potential to improve colorectal cancer screening. Scientific Reports, 11(1). https://doi.org/10.1038/s41598-021-99046-w
Leng, Q., Holden, V. K., Deepak, J., Todd, N. W., & Jiang, F. (2021). Microbiota Biomarkers for Lung Cancer. Diagnostics, 11(3), 407. https://doi.org/10.3390/diagnostics11030407
Liang, J. Q., Li, T., Nakatsu, G., Chen, Y.-X., Yau, T. O., Chu, E., Wong, S., Szeto, C. H., Ng, S. C., Chan, F. K. L., Fang, J.-Y., Sung, J. J. Y., & Yu, J. (2019). A novel faecal Lachnoclostridium marker for the non-invasive diagnosis of colorectal adenoma and cancer. Gut, 69(7), 1248-1257. https://doi.org/10.1136/gutjnl-2019-318532
Louis, P., Hold, G. L., & Flint, H. J. (2014). The gut microbiota, bacterial metabolites and colorectal cancer. Nature Reviews. Microbiology, 12(10), 661-672. https://doi.org/10.1038/nrmicro3344
Mager, D., Haffajee, A., Devlin, P., Norris, C., Posner, M., & Goodson, J. (2005). The salivary microbiota as a diagnostic indicator of oral cancer: A descriptive, non-randomized study of cancer-free and oral squamous cell carcinoma subjects. Journal of Translational Medicine, 3(1), 27. https://doi.org/10.1186/1479-5876-3-27
Manzoor, S. S., Doedens, A., & Burns, M. B. (2020). The promise and challenge of cancer microbiome research. Genome Biology, 21(1). https://doi.org/10.1186/s13059-020-02037-9
Marmorino, F., Piccinno, G., Rossini, D., Ghelardi, F., Murgioni, S., Salvatore, L., Nasca, V., Antoniotti, C., Daniel, F., Schietroma, F., Conca, V., Alves, C., Tamburini, E., Tamberi, S., Passardi, A., Antonuzzo, L., D'Onofrio, R., Zitvogel, L., Cremolini, C., & Derosa, L. (2023). Gut microbiome composition as predictor of the efficacy of adding atezolizumab to first-line FOLFOXIRI plus bevacizumab in metastatic colorectal cancer: A translational analysis of the AtezoTRIBE study. Journal of Clinical Oncology, 41(16_suppl), 3534-3534. https://doi.org/10.1200/JCO.2023.41.16_suppl.3534
Mitra, A., MacIntyre, D. A., Marchesi, J. R., Lee, Y. S., Bennett, P. R., & Kyrgiou, M. (2016). The vaginal microbiota, human papillomavirus infection and cervical intraepithelial neoplasia: what do we know and where are we going next? Microbiome, 4(1). https://doi.org/10.1186/s40168-016-0203-0
Moreno-Gonzalez, M., & Beraza, N. (2021). The Role of the Microbiome in Liver Cancer. Cancers, 13(10), 2330. https://doi.org/10.3390/cancers13102330
Mukherji, R., & Weinberg, B. A. (2020). The gut microbiome and potential implications for early-onset colorectal cancer. Colorectal Cancer, 9(3), CRC25. https://doi.org/10.2217/crc-2020-0007
Negrut, R. L., Cote, A., & Adrian Marius Maghiar. (2023). Exploring the Potential of Oral Microbiome Biomarkers for Colorectal Cancer Diagnosis and Prognosis: A Systematic Review. Microorganisms, 11(6), 1586-1586. https://doi.org/10.3390/microorganisms11061586
Olovo, C. V., Huang, X., Zheng, X., & Xu, M. (2021). Faecal microbial biomarkers in early diagnosis of colorectal cancer. Journal of Cellular and Molecular Medicine, 25(23), 10783-10797. https://doi.org/10.1111/jcmm.17010
Parhi, L., Alon-Maimon, T., Sol, A., Nejman, D., Shhadeh, A., Fainsod-Levi, T., Yajuk, O., Isaacson, B., Abed, J., Maalouf, N., Nissan, A., Sandbank, J., Yehuda-Shnaidman, E., Ponath, F., Vogel, J., Mandelboim, O., Granot, Z., Straussman, R., & Bachrach, G. (2020). Breast cancer colonization by Fusobacterium nucleatum accelerates tumor growth and metastatic progression. Nature Communications, 11(1). https://doi.org/10.1038/s41467-020-16967-2
Parida, S., & Sharma, D. (2021). The Microbiome and Cancer: Creating Friendly Neighborhoods and Removing the Foes Within A C. Cancer Research, 81(4). https://doi.org/10.1158/0008-5472.CAN-20-2629
Pasolli, E., Truong, D. T., Malik, F., Waldron, L., & Segata, N. (2016). Machine Learning Meta-analysis of Large Metagenomic Datasets: Tools and Biological Insights. PLoS Computational Biology, 12(7). https://doi.org/10.1371/journal.pcbi.1004977
Pasquereau-Kotula, E., Martins, M., Aymeric, L., & Dramsi, S. (2018). Significance of Streptococcus gallolyticus subsp. gallolyticus Association With Colorectal Cancer. Frontiers in Microbiology, 9. https://doi.org/10.3389/fmicb.2018.00614
Pegg, A. E. (2009). Mammalian polyamine metabolism and function. IUBMB Life, 61(9), 880-894. https://doi.org/10.1002/iub.230
Peng, L., Li, Z.-R., Green, R. S., Holzman, I. R., & Lin, J. (2009). Butyrate Enhances the Intestinal Barrier by Facilitating Tight Junction Assembly via Activation of AMP-Activated Protein Kinase in Caco-2 Cell Monolayers. The Journal of Nutrition, 139(9), 1619-1625. https://doi.org/10.3945/jn.109.104638
Ramírez-Labrada, A. G., Isla, D., Artal, A., Arias, M., Rezusta, A., Pardo, J., & Gálvez, E. M. (2020). The Influence of Lung Microbiota on Lung Carcinogenesis, Immunity, and Immunotherapy. Trends in Cancer, 6(2), 86-97. https://doi.org/10.1016/j.trecan.2019.12.007
Rooks, M. G., & Garrett, W. S. (2016). Gut microbiota, metabolites and host immunity. Nature Reviews Immunology, 16(6), 341-352. https://doi.org/10.1038/nri.2016.42
Schmidt, B. L., Kuczynski, J., Bhattacharya, A., Huey, B., Corby, P. M., Queiroz, E. L. S., Nightingale, K., Kerr, A. R., DeLacure, M. D., Veeramachaneni, R., Olshen, A. B., & Albertson, D. G. (2014). Changes in Abundance of Oral Microbiota Associated with Oral Cancer. PLoS ONE, 9(6), e98741. https://doi.org/10.1371/journal.pone.0098741
Schwabe, R. F., & Jobin, C. (2013). The microbiome and cancer. Nature Reviews Cancer, 13(11), 800-812. https://doi.org/10.1038/nrc3610
Shrestha, E., White, J. R., Yu, S.-H., Kulac, I., Ertunc, O., De Marzo, A. M., Yegnasubramanian, S., Mangold, L. A., Partin, A. W., & Sfanos, K. S. (2018). Profiling the Urinary Microbiome in Men with Positive versus Negative Biopsies for Prostate Cancer. Journal of Urology, 199(1), 161-171. https://doi.org/10.1016/j.juro.2017.08.001
Sobhani, I., Tap, J., Roudot-Thoraval, F., Roperch, J. P., Letulle, S., Langella, P., Corthier, G., Van Nhieu, J. T., & Furet, J. P. (2011). Microbial Dysbiosis in Colorectal Cancer (CRC) Patients. PLoS ONE, 6(1), e16393. https://doi.org/10.1371/journal.pone.0016393
Thomas, A. M., Manghi, P., Asnicar, F., Pasolli, E., Armanini, F., Zolfo, M., Beghini, F., Manara, S., Karcher, N., Pozzi, C., Gandini, S., Serrano, D., Tarallo, S., Francavilla, A., Gallo, G., Trompetto, M., Ferrero, G., Mizutani, S., Shiroma, H., & Shiba, S. (2019). Metagenomic analysis of colorectal cancer datasets identifies cross-cohort microbial diagnostic signatures and a link with choline degradation. Nature Medicine, 25(4), 667-678. https://doi.org/10.1038/s41591-019-0405-7
Udayasuryan, B., Ahmad, R. N., Nguyen, T. T. D., Umaña, A., Monét Roberts, L., Sobol, P., Jones, S. D., Munson, J. M., Slade, D. J., & Verbridge, S. S. (2022). Fusobacterium nucleatum induces proliferation and migration in pancreatic cancer cells through host autocrine and paracrine signaling. Science Signaling, 15(756). https://doi.org/10.1126/scisignal.abn4948
Walther-António, M. R. S., Chen, J., Multinu, F., Hokenstad, A., Distad, T. J., Cheek, E. H., Keeney, G. L., Creedon, D. J., Nelson, H., Mariani, A., & Chia, N. (2016). Potential contribution of the uterine microbiome in the development of endometrial cancer. Genome Medicine, 8(1). https://doi.org/10.1186/s13073-016-0368-y
Wang, Z., Klipfell, E., Bennett, B. J., Koeth, R., Levison, B. S., DuGar, B., Feldstein, A. E., Britt, E. B., Fu, X., Chung, Y.-M., Wu, Y., Schauer, P., Smith, J. D., Allayee, H., Tang, W. H. W., DiDonato, J. A., Lusis, A. J., & Hazen, S. L. (2011). Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature, 472(7341), 57-63. https://doi.org/10.1038/nature09922
Warnke-Sommer, J. D., & Ali, H. H. (2017). Evaluation of the oral microbiome as a biomarker for early detection of human oral carcinomas. Proceedings - 2017 IEEE International Conference on Bioinformatics and Biomedicine, BIBM. https://doi.org/10.1109/BIBM.2017.8217979
Wirbel, J., Pyl, P. T., Kartal, E., Zych, K., Kashani, A., Milanese, A., Fleck, J. S., Voigt, A. Y., Palleja, A., Ponnudurai, R., Sunagawa, S., Coelho, L. P., Schrotz-King, P., Vogtmann, E., Habermann, N., Niméus, E., Thomas, A. M., Manghi, P., Gandini, S., & Serrano, D. (2019). Meta-analysis of fecal metagenomes reveals global microbial signatures that are specific for colorectal cancer. Nature Medicine, 25(4), 679-689. https://doi.org/10.1038/s41591-019-0406-6
Xie, Y.-H., Gao, Q.-Y., Cai, G.-X., Sun, X.-M., Xm, S., Th, Z., Hm, C., Sy, Y., Yw, Q., Wq, G., Xy, C., Y, C., D, S., Zj, L., Sj, C., J, X., Yx, C., & Jy, F. (2017). Fecal Clostridium symbiosum for Noninvasive Detection of Early and Advanced Colorectal Cancer: Test and Validation Studies. EBioMedicine, 25. https://doi.org/10.1016/j.ebiom.2017.10.005
Xuan, C., Shamonki, J. M., Chung, A., DiNome, M. L., Chung, M., Sieling, P. A., & Lee, D. J. (2014). Microbial Dysbiosis Is Associated with Human Breast Cancer. PLoS ONE, 9(1), e83744. https://doi.org/10.1371/journal.pone.0083744
Yang, X., Da, M., Zhang, W., Qi, Q., Zhang, C., & Han, S. (2018). Role of Lactobacillus in cervical cancer. Cancer Management and Research, 10, 1219-1229. https://doi.org/10.2147/CMAR.S165228
Yan, X., Yang, M., Liu, J., Gao, R., Hu, J., Li, J., Zhang, L., Shi, Y., Guo, H., Cheng, J., Razi, M., Pang, S., Yu, X., & Hu, S. (2015). Discovery and validation of potential bacterial biomarkers for lung cancer. American journal of cancer research, 5(10), 3111-3122.
Yao, Y., Ni, H., Wang, X., Xu, Q., Zhang, J., Jiang, L., Wang, B., Song, S., & Zhu, X. (2021). A New Biomarker of Fecal Bacteria for Non-Invasive Diagnosis of Colorectal Cancer. Frontiers in Cellular and Infection Microbiology, 11. https://doi.org/10.3389/fcimb.2021.744049
Yu, J., Feng, Q., Wong, S. H., Zhang, D., Liang, Q. yi, Qin, Y., Tang, L., Zhao, H., Stenvang, J., Li, Y., Wang, X., Xu, X., Chen, N., Wu, W. K. K., Al-Aama, J., Nielsen, H. J., Kiilerich, P., Jensen, B. A. H., Yau, T. O., & Lan, Z. (2015). Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer. Gut, 66(1), 70-78. https://doi.org/10.1136/gutjnl-2015-309800
Zackular, J. P., Baxter, N. T., Iverson, K. D., Sadler, W. D., Petrosino, J. F., Chen, G. Y., & Schloss, P. D. (2013). The Gut Microbiome Modulates Colon Tumorigenesis. MBio, 4(6). https://doi.org/10.1128/mBio.00692-13
Zeller, G., Tap, J., Voigt, A. Y., Sunagawa, S., Kultima, J. R., Costea, P. I., Amiot, A., Böhm, J., Brunetti, F., Habermann, N., Hercog, R., Koch, M., Luciani, A., Mende, D. R., Schneider, M. A., Schrotz-King, P., Tournigand, C., Tran Van Nhieu, J., Yamada, T., & Zimmermann, J. (2014). Potential of fecal microbiota for early-stage detection of colorectal cancer. Molecular Systems Biology, 10(11). https://doi.org/10.15252/msb.20145645
Zheng, Y., Fang, Z., Xue, Y., Zhang, J., Zhu, J., Gao, R., Yao, S., Ye, Y., Wang, S., Lin, C., Chen, S., Huang, H., Hu, L., Jiang, G.-N., Qin, H., Zhang, P., Chen, J., & Ji, H. (2020). Specific gut microbiome signature predicts the early-stage lung cancer. Gut Microbes, 11(4), 1030-1042. https://doi.org/10.1080/19490976.2020.1737487
Zhu, W., Shen, W., Wang, J., Xu, Y., Zhai, R., Zhang, J., Wang, M., Wang, M., & Liu, L. (2022). Capnocytophaga gingivalis is a potential tumor promotor in oral cancer. Oral Diseases. https://doi.org/10.1111/odi.14376
Zwezerijnen-Jiwa, F. H., Sivov, H., Paizs, P., Zafeiropoulou, K., & Kinross, J. (2022). A systematic review of microbiome-derived biomarkers for early colorectal cancer detection. Neoplasia (New York, N.Y.), 36, 100868. https://doi.org/10.1016/j.neo.2022.100868
Downloads
Published
Issue
Section
License
Copyright (c) 2025 Mikrobiolohichnyi Zhurnal
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
