Review
. 2019 Jun; 143:255-294.
doi: 10.1016/bs.acr.2019.03.005.

Impact of the microbiome on cancer progression and response to anti-cancer therapies

Claire Buchta Rosean 1 Tzu-Yu Feng 1 Francesca N Azar 1 Melanie R Rutkowski 2 
Affiliations
  • PMID: 31202360
  •     183 References
  •     9 citations

Abstract

Humans are a colonized with trillions of commensal microorganisms which exert a profound effect on normal host physiology and immune function through an abundance of genetic and metabolic by-products. Although the commensal microbiome has beneficial functions to host physiology, perturbations of the composition of the commensal microbiome or the homeostatic mucosal environment can lead to the induction of immune pathology and systemic inflammation. In the context of cancer progression or response to immune therapy, this inflammation can be detrimental, resulting in tumor growth and the promotion of immune suppression. On the other hand, significant associations have been identified whereby certain commensal microorganisms are able to enhance T cell function or are required for tumor control in cancer patients treated with certain immune therapies and chemotherapies. The focus of this chapter is to highlight the role of the commensal microbiome during tumor progression and in response to immune therapies.

Keywords: Cancer; Commensal dysbiosis; Immunosuppression; Immunotherapy; Microbiome.

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Michael H Shaw, Nobuhiko Kamada, Yun-Gi Kim, Gabriel Núñez.
J Exp Med, 2012 Feb 01; 209(2). PMID: 22291094    Free PMC article.
Highly Cited.
The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota.
June L Round, S Melanie Lee, +4 authors, Sarkis K Mazmanian.
Science, 2011 Apr 23; 332(6032). PMID: 21512004    Free PMC article.
Highly Cited.
The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients.
Vyara Matson, Jessica Fessler, +5 authors, Thomas F Gajewski.
Science, 2018 Jan 06; 359(6371). PMID: 29302014    Free PMC article.
Highly Cited.
Fusobacterium is associated with colorectal adenomas.
Amber N McCoy, Félix Araújo-Pérez, +3 authors, Temitope O Keku.
PLoS One, 2013 Jan 22; 8(1). PMID: 23335968    Free PMC article.
Highly Cited.
Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients.
V Gopalakrishnan, C N Spencer, +67 authors, J A Wargo.
Science, 2017 Nov 04; 359(6371). PMID: 29097493    Free PMC article.
Highly Cited.
Tumour-associated and non-tumour-associated microbiota in colorectal cancer.
Burkhardt Flemer, Denise B Lynch, +6 authors, Paul W O'Toole.
Gut, 2016 Mar 20; 66(4). PMID: 26992426    Free PMC article.
Highly Cited.
Microbial exposure during early life has persistent effects on natural killer T cell function.
Torsten Olszak, Dingding An, +8 authors, Richard S Blumberg.
Science, 2012 Mar 24; 336(6080). PMID: 22442383    Free PMC article.
Highly Cited.
Duodenal infusion of donor feces for recurrent Clostridium difficile.
Els van Nood, Anne Vrieze, +10 authors, Josbert J Keller.
N Engl J Med, 2013 Jan 18; 368(5). PMID: 23323867
Highly Cited.
Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy.
Ayelet Sivan, Leticia Corrales, +9 authors, Thomas F Gajewski.
Science, 2015 Nov 07; 350(6264). PMID: 26541606    Free PMC article.
Highly Cited.
Cervicovaginal microbiome dysbiosis is associated with proteome changes related to alterations of the cervicovaginal mucosal barrier.
H Borgdorff, R Gautam, +6 authors, J H H M van de Wijgert.
Mucosal Immunol, 2015 Sep 10; 9(3). PMID: 26349657
Highly Cited.
Dysbiosis of gut microbiota in promoting the development of colorectal cancer.
Shaomin Zou, Lekun Fang, Mong-Hong Lee.
Gastroenterol Rep (Oxf), 2018 Feb 27; 6(1). PMID: 29479437    Free PMC article.
Highly Cited. Review.
Succession of microbial consortia in the developing infant gut microbiome.
Jeremy E Koenig, Aymé Spor, +5 authors, Ruth E Ley.
Proc Natl Acad Sci U S A, 2010 Jul 30; 108 Suppl 1. PMID: 20668239    Free PMC article.
Highly Cited.
The human microbiome project.
Peter J Turnbaugh, Ruth E Ley, +3 authors, Jeffrey I Gordon.
Nature, 2007 Oct 19; 449(7164). PMID: 17943116    Free PMC article.
Highly Cited.
Clinical evaluation of CpG oligonucleotides as adjuvants for vaccines targeting infectious diseases and cancer.
Julia Scheiermann, Dennis M Klinman.
Vaccine, 2014 Jul 01; 32(48). PMID: 24975812    Free PMC article.
Highly Cited. Review.
Redirecting in vivo elicited tumor infiltrating macrophages and dendritic cells towards tumor rejection.
Cristiana Guiducci, Alain P Vicari, +2 authors, Mario P Colombo.
Cancer Res, 2005 Apr 19; 65(8). PMID: 15833879
Highly Cited.
The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice.
Premysl Bercik, Emmanuel Denou, +9 authors, Stephen M Collins.
Gastroenterology, 2011 Jun 21; 141(2). PMID: 21683077
Highly Cited.
Role of the gut microbiota in immunity and inflammatory disease.
Nobuhiko Kamada, Sang-Uk Seo, Grace Y Chen, Gabriel Núñez.
Nat Rev Immunol, 2013 Apr 27; 13(5). PMID: 23618829
Highly Cited. Review.
Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity.
Thomas B Clarke, Kimberly M Davis, +3 authors, Jeffrey N Weiser.
Nat Med, 2010 Jan 19; 16(2). PMID: 20081863    Free PMC article.
Highly Cited.
Microbial colonization drives expansion of IL-1 receptor 1-expressing and IL-17-producing gamma/delta T cells.
Jinyou Duan, Hachung Chung, Erin Troy, Dennis L Kasper.
Cell Host Microbe, 2010 Feb 18; 7(2). PMID: 20159619    Free PMC article.
Effects of vendor and genetic background on the composition of the fecal microbiota of inbred mice.
Aaron C Ericsson, J Wade Davis, +5 authors, Craig L Franklin.
PLoS One, 2015 Feb 13; 10(2). PMID: 25675094    Free PMC article.
Highly Cited.
Norovirus gastroenteritis after fecal microbiota transplantation for treatment of Clostridium difficile infection despite asymptomatic donors and lack of sick contacts.
Margot Schwartz, Michael Gluck, Shirley Koon.
Am J Gastroenterol, 2013 Aug 06; 108(8). PMID: 23912408
Tumor-infiltrating CD8+ lymphocytes predict clinical outcome in breast cancer.
Sahar M A Mahmoud, Emma Claire Paish, +5 authors, Andrew R Green.
J Clin Oncol, 2011 Apr 13; 29(15). PMID: 21483002
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Increased GVHD-related mortality with broad-spectrum antibiotic use after allogeneic hematopoietic stem cell transplantation in human patients and mice.
Yusuke Shono, Melissa D Docampo, +30 authors, Robert R Jenq.
Sci Transl Med, 2016 May 20; 8(339). PMID: 27194729    Free PMC article.
Highly Cited.
Airway dysbiosis: Haemophilus influenzae and Tropheryma in poorly controlled asthma.
Jodie L Simpson, Joshua Daly, +8 authors, Peter G Gibson.
Eur Respir J, 2015 Dec 10; 47(3). PMID: 26647445
Regulation of intestinal inflammation by microbiota following allogeneic bone marrow transplantation.
Robert R Jenq, Carles Ubeda, +18 authors, Marcel R M van den Brink.
J Exp Med, 2012 May 02; 209(5). PMID: 22547653    Free PMC article.
Highly Cited.
Immune-related gene signatures predict the outcome of neoadjuvant chemotherapy.
Gautier Stoll, David Enot, +3 authors, Guido Kroemer.
Oncoimmunology, 2014 May 03; 3(1). PMID: 24790795    Free PMC article.
Bacterial lipopolysaccharide directly induces angiogenesis through TRAF6-mediated activation of NF-kappaB and c-Jun N-terminal kinase.
Ingrid Pollet, Christy J Opina, +3 authors, Aly Karsan.
Blood, 2003 Apr 26; 102(5). PMID: 12714497
Temporal bacterial community dynamics vary among ulcerative colitis patients after fecal microbiota transplantation.
Sieglinde Angelberger, Walter Reinisch, +7 authors, David Berry.
Am J Gastroenterol, 2013 Sep 26; 108(10). PMID: 24060759
Highly Cited.
Antitumor therapeutic effects of Salmonella typhimurium containing Flt3 Ligand expression plasmids in melanoma-bearing mouse.
Won Suck Yoon, Won Cheol Choi, Jeong-Im Sin, Yong Keun Park.
Biotechnol Lett, 2007 Jan 20; 29(4). PMID: 17235489
The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide.
Sophie Viaud, Fabiana Saccheri, +30 authors, Laurence Zitvogel.
Science, 2013 Nov 23; 342(6161). PMID: 24264990    Free PMC article.
Highly Cited.
Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment.
Aleksandar D Kostic, Eunyoung Chun, +12 authors, Wendy S Garrett.
Cell Host Microbe, 2013 Aug 21; 14(2). PMID: 23954159    Free PMC article.
Highly Cited.
Revised Estimates for the Number of Human and Bacteria Cells in the Body.
Ron Sender, Shai Fuchs, Ron Milo.
PLoS Biol, 2016 Aug 20; 14(8). PMID: 27541692    Free PMC article.
Highly Cited.
Richness of human gut microbiome correlates with metabolic markers.
Emmanuelle Le Chatelier, Trine Nielsen, +39 authors, Oluf Pedersen.
Nature, 2013 Aug 30; 500(7464). PMID: 23985870
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Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma.
Tyler R Simpson, Fubin Li, +11 authors, Sergio A Quezada.
J Exp Med, 2013 Jul 31; 210(9). PMID: 23897981    Free PMC article.
Highly Cited.
Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors.
Bertrand Routy, Emmanuelle Le Chatelier, +45 authors, Laurence Zitvogel.
Science, 2017 Nov 04; 359(6371). PMID: 29097494
Highly Cited.
Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota.
Marie Vétizou, Jonathan M Pitt, +35 authors, Laurence Zitvogel.
Science, 2015 Nov 07; 350(6264). PMID: 26541610    Free PMC article.
Highly Cited.
MAVS deficiency induces gut dysbiotic microbiota conferring a proallergic phenotype.
Emilie Plantamura, Amiran Dzutsev, +22 authors, Marie-Cecile Michallet.
Proc Natl Acad Sci U S A, 2018 Sep 27; 115(41). PMID: 30249647    Free PMC article.
Lactobacillus supplementation for diarrhoea related to chemotherapy of colorectal cancer: a randomised study.
P Osterlund, T Ruotsalainen, +6 authors, H Joensuu.
Br J Cancer, 2007 Sep 27; 97(8). PMID: 17895895    Free PMC article.
Transfer of gut microbiota from lean and obese mice to antibiotic-treated mice.
Merete Ellekilde, Ellika Selfjord, +9 authors, Camilla H F Hansen.
Sci Rep, 2014 Aug 02; 4. PMID: 25082483    Free PMC article.
The bacteria of periodontal diseases.
W E Moore, L V Moore.
Periodontol 2000, 1994 Jun 01; 5. PMID: 9673163
Highly Cited. Review.
A commensal strain of Staphylococcus epidermidis protects against skin neoplasia.
Teruaki Nakatsuji, Tiffany H Chen, +8 authors, Richard L Gallo.
Sci Adv, 2018 Mar 07; 4(2). PMID: 29507878    Free PMC article.
Highly Cited.
Metagenomic analysis of the stool microbiome in patients receiving allogeneic stem cell transplantation: loss of diversity is associated with use of systemic antibiotics and more pronounced in gastrointestinal graft-versus-host disease.
Ernst Holler, Peter Butzhammer, +16 authors, Peter J Oefner.
Biol Blood Marrow Transplant, 2014 Feb 05; 20(5). PMID: 24492144    Free PMC article.
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Airway microbiota and bronchial hyperresponsiveness in patients with suboptimally controlled asthma.
Yvonne J Huang, Craig E Nelson, +22 authors, National Heart, Lung, and Blood Institute's Asthma Clinical Research Network.
J Allergy Clin Immunol, 2011 Jan 05; 127(2). PMID: 21194740    Free PMC article.
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The tumour microenvironment after radiotherapy: mechanisms of resistance and recurrence.
Holly E Barker, James T E Paget, Aadil A Khan, Kevin J Harrington.
Nat Rev Cancer, 2015 Jun 25; 15(7). PMID: 26105538    Free PMC article.
Highly Cited. Review.
Preclinical rationale for combining radiation therapy and immunotherapy beyond checkpoint inhibitors (i.e., CART).
James P Flynn, Mark H O'Hara, Saumil J Gandhi.
Transl Lung Cancer Res, 2017 May 23; 6(2). PMID: 28529898    Free PMC article.
Review.
Intratumoral delivery and suppression of prostate tumor growth by attenuated Salmonella enterica serovar typhimurium carrying plasmid-based small interfering RNAs.
Ling Zhang, Lifang Gao, +10 authors, De-Qi Xu.
Cancer Res, 2007 Jun 19; 67(12). PMID: 17575154
Engineering the perfect (bacterial) cancer therapy.
Neil S Forbes.
Nat Rev Cancer, 2010 Oct 15; 10(11). PMID: 20944664    Free PMC article.
Highly Cited. Review.
Maternal IgG and IgA Antibodies Dampen Mucosal T Helper Cell Responses in Early Life.
Meghan A Koch, Gabrielle L Reiner, +6 authors, Gregory M Barton.
Cell, 2016 May 08; 165(4). PMID: 27153495    Free PMC article.
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Randomized study of the effect of synbiotics during neoadjuvant chemotherapy on adverse events in esophageal cancer patients.
Masaaki Motoori, Masahiko Yano, +15 authors, Masato Sakon.
Clin Nutr, 2015 Dec 09; 36(1). PMID: 26644166
Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome.
Shin Yoshimoto, Tze Mun Loo, +12 authors, Naoko Ohtani.
Nature, 2013 Jun 28; 499(7456). PMID: 23803760
Highly Cited.
Pretreatment with Saccharomyces boulardii does not prevent the experimental mucositis in Swiss mice.
Tatiani Uceli Maioli, Brenda de Melo Silva, +6 authors, Simone de Vasconcelos Generoso.
J Negat Results Biomed, 2014 Apr 12; 13. PMID: 24721659    Free PMC article.
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Erika Vacchelli, Ilio Vitale, +6 authors, Lorenzo Galluzzi.
Oncoimmunology, 2013 Dec 10; 2(9). PMID: 24319634    Free PMC article.
Review.
Salmonella engineered to express CD20-targeting antibodies and a drug-converting enzyme can eradicate human lymphomas.
Paul E Massa, Aida Paniccia, +2 authors, Maria Rescigno.
Blood, 2013 Jun 06; 122(5). PMID: 23736700
Microbial regulation of intestinal radiosensitivity.
Peter A Crawford, Jeffrey I Gordon.
Proc Natl Acad Sci U S A, 2005 Sep 01; 102(37). PMID: 16129828    Free PMC article.
Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens.
Mark E Dudley, James C Yang, +17 authors, Steven A Rosenberg.
J Clin Oncol, 2008 Sep 24; 26(32). PMID: 18809613    Free PMC article.
Highly Cited.
Short hairpin RNA-expressing bacteria elicit RNA interference in mammals.
Shuanglin Xiang, Johannes Fruehauf, Chiang J Li.
Nat Biotechnol, 2006 May 16; 24(6). PMID: 16699500
Population-level analysis of gut microbiome variation.
Gwen Falony, Marie Joossens, +24 authors, Jeroen Raes.
Science, 2016 Apr 30; 352(6285). PMID: 27126039
Highly Cited.
Low-Dose Cyclophosphamide Induces Antitumor T-Cell Responses, which Associate with Survival in Metastatic Colorectal Cancer.
Martin Scurr, Tom Pembroke, +13 authors, Andrew Godkin.
Clin Cancer Res, 2017 Sep 01; 23(22). PMID: 28855352    Free PMC article.
Orogenital contact: a cause of chorioamnionitis?
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Obstet Gynecol, 1994 Oct 01; 84(4 Pt 2). PMID: 9205437
Current understanding of the human microbiome.
Jack A Gilbert, Martin J Blaser, +3 authors, Rob Knight.
Nat Med, 2018 Apr 11; 24(4). PMID: 29634682    Free PMC article.
Highly Cited. Review.
Tumor immune profiling predicts response to anti-PD-1 therapy in human melanoma.
Adil I Daud, Kimberly Loo, +15 authors, Michael D Rosenblum.
J Clin Invest, 2016 Aug 16; 126(9). PMID: 27525433    Free PMC article.
Highly Cited.
Radiation induces proinflammatory dysbiosis: transmission of inflammatory susceptibility by host cytokine induction.
Shiran Gerassy-Vainberg, Alexandra Blatt, +11 authors, Yehuda Chowers.
Gut, 2017 Apr 26; 67(1). PMID: 28438965
The multifaceted role of commensal microbiota in homeostasis and gastrointestinal diseases.
Marcelo José Barbosa Silva, Matheus Batista Heitor Carneiro, +3 authors, Liliane Martins dos Santos.
J Immunol Res, 2015 Mar 12; 2015. PMID: 25759839    Free PMC article.
Review.
Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells.
Yukihiro Furusawa, Yuuki Obata, +27 authors, Hiroshi Ohno.
Nature, 2013 Nov 15; 504(7480). PMID: 24226770
Highly Cited.
Gut microbiota promote hematopoiesis to control bacterial infection.
Arya Khosravi, Alberto Yáñez, +4 authors, Sarkis K Mazmanian.
Cell Host Microbe, 2014 Mar 19; 15(3). PMID: 24629343    Free PMC article.
Highly Cited.
The Treatment of Inoperable Sarcoma by Bacterial Toxins (the Mixed Toxins of the Streptococcus erysipelas and the Bacillus prodigiosus).
W B Coley.
Proc R Soc Med, 1910 Jan 01; 3(Surg Sect). PMID: 19974799    Free PMC article.
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Intraluminal Flagellin Differentially Contributes to Gut Dysbiosis and Systemic Inflammation following Burn Injury.
Logan Grimes, Allie Doyle, +5 authors, Tonyia Eaves-Pyles.
PLoS One, 2016 Dec 03; 11(12). PMID: 27907005    Free PMC article.
Induction of intestinal Th17 cells by segmented filamentous bacteria.
Ivaylo I Ivanov, Koji Atarashi, +14 authors, Dan R Littman.
Cell, 2009 Oct 20; 139(3). PMID: 19836068    Free PMC article.
Highly Cited.
Gut microbial dysbiosis may predict diarrhea and fatigue in patients undergoing pelvic cancer radiotherapy: a pilot study.
Aiping Wang, Zongxin Ling, +10 authors, Junping Wang.
PLoS One, 2015 May 09; 10(5). PMID: 25955845    Free PMC article.
Microbially driven TLR5-dependent signaling governs distal malignant progression through tumor-promoting inflammation.
Melanie R Rutkowski, Tom L Stephen, +12 authors, Jose R Conejo-Garcia.
Cancer Cell, 2014 Dec 24; 27(1). PMID: 25533336    Free PMC article.
Highly Cited.
Attenuated Salmonella engineered to produce human cytokine LIGHT inhibit tumor growth.
Markus Loeffler, Gaelle Le'Negrate, Maryla Krajewska, John C Reed.
Proc Natl Acad Sci U S A, 2007 Jul 27; 104(31). PMID: 17652173    Free PMC article.
Prognostic Effect of Tumor Lymphocytic Infiltration in Resectable Non-Small-Cell Lung Cancer.
Elisabeth Brambilla, Gwénaël Le Teuff, +14 authors, Ming Sound Tsao.
J Clin Oncol, 2016 Feb 03; 34(11). PMID: 26834066    Free PMC article.
Highly Cited.
Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment.
Noriho Iida, Amiran Dzutsev, +18 authors, Romina S Goldszmid.
Science, 2013 Nov 23; 342(6161). PMID: 24264989    Free PMC article.
Highly Cited.
Use of probiotics for prevention of radiation-induced diarrhea.
P Delia, G Sansotta, +4 authors, G Famularo.
World J Gastroenterol, 2007 Mar 14; 13(6). PMID: 17352022    Free PMC article.
The future of immune checkpoint therapy.
Padmanee Sharma, James P Allison.
Science, 2015 Apr 04; 348(6230). PMID: 25838373
Highly Cited. Review.
Environment dominates over host genetics in shaping human gut microbiota.
Daphna Rothschild, Omer Weissbrod, +26 authors, Eran Segal.
Nature, 2018 Mar 01; 555(7695). PMID: 29489753
Highly Cited.
[Update on HPV-associated head and neck cancer-highlights from the 2019 ASCO Annual Meeting].
S Tribius, N Würdemann, +3 authors, J P Klussmann.
HNO, 2019 Nov 09; 67(12). PMID: 31701169
Review.
Oncobiosis and Microbial Metabolite Signaling in Pancreatic Adenocarcinoma.
Borbála Kiss, Edit Mikó, +6 authors, Péter Árkosy.
Cancers (Basel), 2020 Apr 30; 12(5). PMID: 32344895    Free PMC article.
Review.
The Microbiome as a Component of the Tumor Microenvironment.
Tünde Kovács, Edit Mikó, +2 authors, Péter Bai.
Adv Exp Med Biol, 2020 Feb 08; 1225. PMID: 32030653
Review.
Research Progress of Pancreas-Related Microorganisms and Pancreatic Cancer.
Wenqing Zhang, Kunpeng Zhang, +3 authors, Xiaoyu Li.
Front Oncol, 2021 Feb 02; 10. PMID: 33520714    Free PMC article.
Review.
Gut microbiome, Vitamin D, ACE2 interactions are critical factors in immune-senescence and inflammaging: key for vaccine response and severity of COVID-19 infection.
Santosh Shenoy.
Inflamm Res, 2021 Nov 06; 71(1). PMID: 34738147    Free PMC article.
Review.
Prospects and Challenges of the Study of Anti-Glycan Antibodies and Microbiota for the Monitoring of Gastrointestinal Cancer.
Eugeniy P Smorodin.
Int J Mol Sci, 2021 Nov 14; 22(21). PMID: 34769037    Free PMC article.
Review.
The involvement of oncobiosis and bacterial metabolite signaling in metastasis formation in breast cancer.
Tünde Kovács, Edit Mikó, +4 authors, Peter Bai.
Cancer Metastasis Rev, 2021 Dec 31; 40(4). PMID: 34967927    Free PMC article.
Review.
Exploiting the Metabolism of the Gut Microbiome as a Vehicle for Targeted Drug Delivery to the Colon.
Hamid A Bakshi, Gerry A Quinn, +8 authors, Murtaza M Tambuwala.
Pharmaceuticals (Basel), 2021 Dec 29; 14(12). PMID: 34959610    Free PMC article.
Review.
Intratumor microbiome in cancer progression: current developments, challenges and future trends.
Jinyan Liu, Yi Zhang.
Biomark Res, 2022 Jun 02; 10(1). PMID: 35642013
Review.