Gastrectomy impact on the gut microbiome in patients with gastric cancer: A comprehensive review

Vaidota Maksimaityte, Augustinas Bausys, Marius Kryzauskas, Martynas Luksta, Ieva Stundiene, Klaudija Bickaite, Bernardas Bausys, Tomas Poskus, Rimantas Bausys, Kestutis Strupas, Vaidota Maksimaityte, Augustinas Bausys, Marius Kryzauskas, Martynas Luksta, Ieva Stundiene, Klaudija Bickaite, Bernardas Bausys, Tomas Poskus, Rimantas Bausys, Kestutis Strupas

Abstract

Gastric cancer is one of the most common malignancies worldwide and gastrectomy remains the only potentially curative treatment option for this disease. However, the surgery leads to significant physiological and anatomical changes in the gastrointestinal (GI) tract including loss of the gastric barrier, an increase in oxygenation levels in the distal gut, and biliary diversion after gastrectomy. These changes in the GI tract influence the composition of the gut microbiome and thus, host health. Gastrectomy-induced dysbiosis is characterized by increased abundance of typical oral cavity bacteria, an increase in aero-tolerant bacteria (aerobes/facultative anaerobes), and increased abundance of bile acid-transforming bacteria. Furthermore, this dysbiosis is linked to intestinal inflammation, small intestinal bacterial overgrowth, various GI symptoms, and an increased risk of colorectal cancer.

Keywords: Comprehensive review; Dysbiosis; Gastrectomy; Gastric cancer; Gut microbiota; Microbiome.

Conflict of interest statement

Conflict-of-interest statement: The authors declare no conflicts of interest.

©The Author(s) 2021. Published by Baishideng Publishing Group Inc. All rights reserved.

Figures

Figure 1
Figure 1
Gastrectomy impact on the gastrointestinal tract environment and gut microbiome.

References

    1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.
    1. Stratilatovas E, Baušys A, Baušys R, Sangaila E. Mortality after gastrectomy: a 10 year single institution experience. Acta Chir Belg. 2015;115:123–130.
    1. Yu W, Park KB, Chung HY, Kwon OK, Lee SS. Chronological Changes of Quality of Life in Long-Term Survivors after Gastrectomy for Gastric Cancer. Cancer Res Treat. 2016;48:1030–1036.
    1. Lee SS, Chung HY, Kwon OK, Yu W. Quality of life in cancer survivors 5 years or more after total gastrectomy: a case-control study. Int J Surg. 2014;12:700–705.
    1. Brenkman HJF, Tegels JJW, Ruurda JP, Luyer MDP, Kouwenhoven EA, Draaisma WA, van der Peet DL, Wijnhoven BPL, Stoot JHMB, van Hillegersberg R LOGICA Study Group. Factors influencing health-related quality of life after gastrectomy for cancer. Gastric Cancer. 2018;21:524–532.
    1. Erawijantari PP, Mizutani S, Shiroma H, Shiba S, Nakajima T, Sakamoto T, Saito Y, Fukuda S, Yachida S, Yamada T. Influence of gastrectomy for gastric cancer treatment on faecal microbiome and metabolome profiles. Gut. 2020;69:1404–1415.
    1. Ikeda Y, Saku M, Kawanaka H, Nonaka M, Yoshida K. Features of second primary cancer in patients with gastric cancer. Oncology. 2003;65:113–117.
    1. Eom BW, Lee HJ, Yoo MW, Cho JJ, Kim WH, Yang HK, Lee KU. Synchronous and metachronous cancers in patients with gastric cancer. J Surg Oncol. 2008;98:106–110.
    1. Bäumler AJ, Sperandio V. Interactions between the microbiota and pathogenic bacteria in the gut. Nature. 2016;535:85–93.
    1. Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: an integrative view. Cell. 2012;148:1258–1270.
    1. Bliss ES, Whiteside E. The Gut-Brain Axis, the Human Gut Microbiota and Their Integration in the Development of Obesity. Front Physiol. 2018;9:900.
    1. Shreiner AB, Kao JY, Young VB. The gut microbiome in health and in disease. Curr Opin Gastroenterol. 2015;31:69–75.
    1. Zhan X, Stamova B, Jin LW, DeCarli C, Phinney B, Sharp FR. Gram-negative bacterial molecules associate with Alzheimer disease pathology. Neurology. 2016;87:2324–2332.
    1. Zhao Y, Jaber V, Lukiw WJ. Secretory Products of the Human GI Tract Microbiome and Their Potential Impact on Alzheimer's Disease (AD): Detection of Lipopolysaccharide (LPS) in AD Hippocampus. Front Cell Infect Microbiol. 2017;7:318.
    1. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, de Vos WM, Cani PD. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci USA. 2013;110:9066–9071.
    1. Li J, Butcher J, Mack D, Stintzi A. Functional impacts of the intestinal microbiome in the pathogenesis of inflammatory bowel disease. Inflamm Bowel Dis. 2015;21:139–153.
    1. Mondot S, Kang S, Furet JP, Aguirre de Carcer D, McSweeney C, Morrison M, Marteau P, Doré J, Leclerc M. Highlighting new phylogenetic specificities of Crohn's disease microbiota. Inflamm Bowel Dis. 2011;17:185–192.
    1. Wei B, Su TT, Dalwadi H, Stephan RP, Fujiwara D, Huang TT, Brewer S, Chen L, Arditi M, Borneman J, Rawlings DJ, Braun J. Resident enteric microbiota and CD8+ T cells shape the abundance of marginal zone B cells. Eur J Immunol. 2008;38:3411–3425.
    1. Wu S, Rhee KJ, Albesiano E, Rabizadeh S, Wu X, Yen HR, Huso DL, Brancati FL, Wick E, McAllister F, Housseau F, Pardoll DM, Sears CL. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med. 2009;15:1016–1022.
    1. Karakan T, Ozkul C, Küpeli Akkol E, Bilici S, Sobarzo-Sánchez E, Capasso R. Gut-Brain-Microbiota Axis: Antibiotics and Functional Gastrointestinal Disorders. Nutrients. 2021;13
    1. Liou AP, Paziuk M, Luevano JM Jr, Machineni S, Turnbaugh PJ, Kaplan LM. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med. 2013;5:178ra41.
    1. Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y, Brach T, Liang S, Feng Q, Jørgensen NB, Bojsen-Møller KN, Dirksen C, Burgdorf KS, Holst JJ, Madsbad S, Wang J, Pedersen O, Hansen T, Arumugam M. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med. 2016;8:67.
    1. Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, Parameswaran P, Crowell MD, Wing R, Rittmann BE, Krajmalnik-Brown R. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci USA. 2009;106:2365–2370.
    1. Karami R, Kermansaravi M, Pishgahroudsari M, Talebi M, Mohammadzadeh N, Pazouki A. Changes in gut microbial flora after Roux-en-Y gastric bypass and sleeve gastrectomy and their effects on post-operative weight loss. Updates Surg. 2020
    1. Xu G, Song M. Recent advances in the mechanisms underlying the beneficial effects of bariatric and metabolic surgery. Surg Obes Relat Dis. 2021;17:231–238.
    1. Sanchez-Carrillo S, Ciordia S, Rojo D, Zubeldia-Varela E, Méndez-García C, Martínez-Martínez M, Barbas C, Ruiz-Ruiz S, Moya A, Garriga M, Salazar N, Botella-Carretero JI, Vega-Piñero B, de Los Reyes-Gavilán CG, Del Campo R, Ferrer M. A body weight loss- and health-promoting gut microbiota is established after bariatric surgery in individuals with severe obesity. J Pharm Biomed Anal. 2021;193:113747.
    1. Horvath A, Bausys A, Sabaliauskaite R, Stratilatovas E, Jarmalaite S, Schuetz B, Stiegler P, Bausys R, Stadlbauer V, Strupas K. Distal Gastrectomy with Billroth II Reconstruction is Associated with Oralization of Gut Microbiome and Intestinal Inflammation: A Proof-of-Concept Study. Ann Surg Oncol. 2021;28:1198–1208.
    1. Lin XH, Huang KH, Chuang WH, Luo JC, Lin CC, Ting PH, Young SH, Fang WL, Hou MC, Lee FY. The long term effect of metabolic profile and microbiota status in early gastric cancer patients after subtotal gastrectomy. PLoS One. 2018;13:e0206930.
    1. Liang W, Yang Y, Wang H, Yu X, Lu Y, Shen S, Teng L. Gut microbiota shifts in patients with gastric cancer in perioperative period. Medicine (Baltimore) 2019;98:e16626.
    1. Heiman ML, Greenway FL. A healthy gastrointestinal microbiome is dependent on dietary diversity. Mol Metab. 2016;5:317–320.
    1. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI. A core gut microbiome in obese and lean twins. Nature. 2009;457:480–484.
    1. Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, Al-Soud WA, Sørensen SJ, Hansen LH, Jakobsen M. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One. 2010;5:e9085.
    1. Kowalska-Duplaga K, Gosiewski T, Kapusta P, Sroka-Oleksiak A, Wędrychowicz A, Pieczarkowski S, Ludwig-Słomczyńska AH, Wołkow PP, Fyderek K. Differences in the intestinal microbiome of healthy children and patients with newly diagnosed Crohn's disease. Sci Rep. 2019;9:18880.
    1. Dhakan DB, Maji A, Sharma AK, Saxena R, Pulikkan J, Grace T, Gomez A, Scaria J, Amato KR, Sharma VK. The unique composition of Indian gut microbiome, gene catalogue, and associated fecal metabolome deciphered using multi-omics approaches. Gigascience. 2019;8
    1. Huang L, Xu AM, Li TJ, Han WX, Xu J. Should peri-gastrectomy gastric acidity be our focus among gastric cancer patients? World J Gastroenterol. 2014;20:6981–6988.
    1. Rieu PN, Jansen JB, Hopman WP, Joosten HJ, Lamers CB. Effect of partial gastrectomy with Billroth II or Roux-en-Y anastomosis on postprandial and cholecystokinin-stimulated gallbladder contraction and secretion of cholecystokinin and pancreatic polypeptide. Dig Dis Sci. 1990;35:1066–1072.
    1. Jepson K, Johnston D. Effect of vagotomy on human gastric acid secretion stimulated by gastrin pentapeptide and by histalog. Gastroenterology. 1968;55:665–669.
    1. Martinsen TC, Bergh K, Waldum HL. Gastric juice: a barrier against infectious diseases. Basic Clin Pharmacol Toxicol. 2005;96:94–102.
    1. Carboni M, Guadagni S, Pistoia MA, Amicucci G, Tuscano D, Negro P, Smith PL, Walters CL. The microflora of the gastric juice after Billroth I and Billroth II partial gastrectomy. Scand J Gastroenterol. 1986;21:461–470.
    1. Horvath A, Rainer F, Bashir M, Leber B, Schmerboeck B, Klymiuk I, Groselj-Strele A, Durdevic M, Freedberg DE, Abrams JA, Fickert P, Stiegler P, Stadlbauer V. Biomarkers for oralization during long-term proton pump inhibitor therapy predict survival in cirrhosis. Sci Rep. 2019;9:12000.
    1. Imhann F, Bonder MJ, Vich Vila A, Fu J, Mujagic Z, Vork L, Tigchelaar EF, Jankipersadsing SA, Cenit MC, Harmsen HJ, Dijkstra G, Franke L, Xavier RJ, Jonkers D, Wijmenga C, Weersma RK, Zhernakova A. Proton pump inhibitors affect the gut microbiome. Gut. 2016;65:740–748.
    1. Bajaj JS, Cox IJ, Betrapally NS, Heuman DM, Schubert ML, Ratneswaran M, Hylemon PB, White MB, Daita K, Noble NA, Sikaroodi M, Williams R, Crossey MM, Taylor-Robinson SD, Gillevet PM. Systems biology analysis of omeprazole therapy in cirrhosis demonstrates significant shifts in gut microbiota composition and function. Am J Physiol Gastrointest Liver Physiol. 2014;307:G951–G957.
    1. Jackson MA, Goodrich JK, Maxan ME, Freedberg DE, Abrams JA, Poole AC, Sutter JL, Welter D, Ley RE, Bell JT, Spector TD, Steves CJ. Proton pump inhibitors alter the composition of the gut microbiota. Gut. 2016;65:749–756.
    1. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE. Defining the normal bacterial flora of the oral cavity. J Clin Microbiol. 2005;43:5721–5732.
    1. Sunakawa Y, Matoba R, Inoue E, Sakamoto Y, Kawabata R, Ishiguro A, Akamaru Y, Kito Y, Takahashi M, Matsuyama J, Yabusaki H, Makiyama A, Suzuki T, Tsuda M, Yasui H, Kawakami H, Muro K, Nakajima TE, Ichikawa W, Fujii M. Genomic pathway of gut microbiome to predict efficacy of nivolumab in advanced gastric cancer: DELIVER trial (JACCRO GC-08) J Clin Oncol . 2021;39:161–161.
    1. Tsuda A, Suda W, Morita H, Takanashi K, Takagi A, Koga Y, Hattori M. Influence of Proton-Pump Inhibitors on the Luminal Microbiota in the Gastrointestinal Tract. Clin Transl Gastroenterol. 2015;6:e89.
    1. Clooney AG, Bernstein CN, Leslie WD, Vagianos K, Sargent M, Laserna-Mendieta EJ, Claesson MJ, Targownik LE. A comparison of the gut microbiome between long-term users and non-users of proton pump inhibitors. Aliment Pharmacol Ther. 2016;43:974–984.
    1. Karanicolas PJ, Graham D, Gönen M, Strong VE, Brennan MF, Coit DG. Quality of life after gastrectomy for adenocarcinoma: a prospective cohort study. Ann Surg. 2013;257:1039–1046.
    1. Kim AR, Cho J, Hsu YJ, Choi MG, Noh JH, Sohn TS, Bae JM, Yun YH, Kim S. Changes of quality of life in gastric cancer patients after curative resection: a longitudinal cohort study in Korea. Ann Surg. 2012;256:1008–1013.
    1. Aoki T, Yamaji I, Hisamoto T, Sato M, Matsuda T. Irregular bowel movement in gastrectomized subjects: bowel habits, stool characteristics, fecal flora, and metabolites. Gastric Cancer. 2012;15:396–404.
    1. Anbazhagan AN, Priyamvada S, Alrefai WA, Dudeja PK. Pathophysiology of IBD associated diarrhea. Tissue Barriers. 2018;6:e1463897.
    1. Qiu Z, Yang H, Rong L, Ding W, Chen J, Zhong L. Targeted Metagenome Based Analyses Show Gut Microbial Diversity of Inflammatory Bowel Disease patients. Indian J Microbiol. 2017;57:307–315.
    1. Yang Q, Huang X, Wang P, Yan Z, Sun W, Zhao S, Gun S. Longitudinal development of the gut microbiota in healthy and diarrheic piglets induced by age-related dietary changes. Microbiologyopen. 2019;8:e923.
    1. Rivière A, Gagnon M, Weckx S, Roy D, De Vuyst L. Mutual Cross-Feeding Interactions between Bifidobacterium longum subsp. longum NCC2705 and Eubacterium rectale ATCC 33656 Explain the Bifidogenic and Butyrogenic Effects of Arabinoxylan Oligosaccharides. Appl Environ Microbiol. 2015;81:7767–7781.
    1. Kaakoush NO. Insights into the Role of Erysipelotrichaceae in the Human Host. Front Cell Infect Microbiol. 2015;5:84.
    1. Celiker H. A new proposed mechanism of action for gastric bypass surgery: Air hypothesis. Med Hypotheses. 2017;107:81–89.
    1. Sachdev AH, Pimentel M. Gastrointestinal bacterial overgrowth: pathogenesis and clinical significance. Ther Adv Chronic Dis. 2013;4:223–231.
    1. Paik CN, Choi MG, Lim CH, Park JM, Chung WC, Lee KM, Jun KH, Song KY, Jeon HM, Chin HM, Park CH, Chung IS. The role of small intestinal bacterial overgrowth in postgastrectomy patients. Neurogastroenterol Motil. 2011;23:e191–e196.
    1. Heinken A, Ravcheev DA, Baldini F, Heirendt L, Fleming RMT, Thiele I. Systematic assessment of secondary bile acid metabolism in gut microbes reveals distinct metabolic capabilities in inflammatory bowel disease. Microbiome. 2019;7:75.
    1. Staley C, Weingarden AR, Khoruts A, Sadowsky MJ. Interaction of gut microbiota with bile acid metabolism and its influence on disease states. Appl Microbiol Biotechnol. 2017;101:47–64.
    1. Yachida S, Mizutani S, Shiroma H, Shiba S, Nakajima T, Sakamoto T, Watanabe H, Masuda K, Nishimoto Y, Kubo M, Hosoda F, Rokutan H, Matsumoto M, Takamaru H, Yamada M, Matsuda T, Iwasaki M, Yamaji T, Yachida T, Soga T, Kurokawa K, Toyoda A, Ogura Y, Hayashi T, Hatakeyama M, Nakagama H, Saito Y, Fukuda S, Shibata T, Yamada T. Metagenomic and metabolomic analyses reveal distinct stage-specific phenotypes of the gut microbiota in colorectal cancer. Nat Med. 2019;25:968–976.
    1. Wirbel J, Pyl PT, Kartal E, Zych K, Kashani A, Milanese A, Fleck JS, Voigt AY, Palleja A, Ponnudurai R, Sunagawa S, Coelho LP, Schrotz-King P, Vogtmann E, Habermann N, Niméus E, Thomas AM, Manghi P, Gandini S, Serrano D, Mizutani S, Shiroma H, Shiba S, Shibata T, Yachida S, Yamada T, Waldron L, Naccarati A, Segata N, Sinha R, Ulrich CM, Brenner H, Arumugam M, Bork P, Zeller G. Meta-analysis of fecal metagenomes reveals global microbial signatures that are specific for colorectal cancer. Nat Med. 2019;25:679–689.
    1. Liu L, Dong W, Wang S, Zhang Y, Liu T, Xie R, Wang B, Cao H. Deoxycholic acid disrupts the intestinal mucosal barrier and promotes intestinal tumorigenesis. Food Funct. 2018;9:5588–5597.
    1. Vich Vila A, Collij V, Sanna S, Sinha T, Imhann F, Bourgonje AR, Mujagic Z, Jonkers DMAE, Masclee AAM, Fu J, Kurilshikov A, Wijmenga C, Zhernakova A, Weersma RK. Impact of commonly used drugs on the composition and metabolic function of the gut microbiota. Nat Commun. 2020;11:362.
    1. Ma W, Mao Q, Xia W, Dong G, Yu C, Jiang F. Gut Microbiota Shapes the Efficiency of Cancer Therapy. Front Microbiol. 2019;10:1050.

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