Skip to main content
Top
Published in: Digestive Diseases and Sciences 5/2019

01-05-2019 | Original Article

Intestinal Microbiota Is Altered in Patients with Gastric Cancer from Shanxi Province, China

Authors: Yu-feng Qi, Jun-ning Sun, Lai-feng Ren, Xue-ling Cao, Jian-hong Dong, Kai Tao, Xue-mei Guan, Ya-ni Cui, Wen Su

Published in: Digestive Diseases and Sciences | Issue 5/2019

Login to get access

Abstract

Background

Many diseases have been associated with intestinal microbial dysbiosis. Host–microbial interactions regulate immune function, which influences the development of gastric cancer.

Aims

The aims were to investigate the characteristics of intestinal microbiota composition in gastric cancer patients and correlations between the intestinal microbiota and cellular immunity.

Methods

Fecal samples were collected from 116 gastric cancer patients and 88 healthy controls from Shanxi Province, China. The intestinal microbiota was investigated by 16S rRNA gene sequencing. Peripheral blood samples were also collected from the 66 gastric cancer patients and 46 healthy controls. The populations of peripheral T lymphocyte subpopulations and NK cells were analyzed by flow cytometry.

Results

The intestinal microbiota in gastric cancer patients was characterized by increased species richness, decreased butyrate-producing bacteria, and the enrichment of other symbiotic bacteria, especially Lactobacillus, Escherichia, and Klebsiella. Lactobacillus and Lachnospira were key species in the network of gastric cancer-associated bacterial genera. The combination of the genera Lachnospira, Lactobacillus, Streptococcus, Veillonella, and Tyzzerella_3 showed good performance in distinguishing gastric cancer patients from healthy controls. There was no significant difference in enterotype distribution between healthy controls and gastric cancer patients. The percentage of CD3+ T cells was positively correlated with the abundance of Lactobacillus and Streptococcus, and CD3+ T cells, CD4+ T cells, and NK cells were associated with Lachnospiraceae taxa.

Conclusions

Our study revealed a dysbiotic intestinal microbiota in gastric cancer patients. The abundance of some intestinal bacterial genera was correlated with the population of peripheral immune cells.
Appendix
Available only for authorised users
Literature
1.
go back to reference Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66:115–132.CrossRefPubMed Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66:115–132.CrossRefPubMed
2.
go back to reference Ferreira RM, Pereira-Marques J, Pinto-Ribeiro I, et al. Gastric microbial community profiling reveals a dysbiotic cancer-associated microbiota. Gut. 2018;67:226–236.CrossRefPubMed Ferreira RM, Pereira-Marques J, Pinto-Ribeiro I, et al. Gastric microbial community profiling reveals a dysbiotic cancer-associated microbiota. Gut. 2018;67:226–236.CrossRefPubMed
3.
go back to reference Hibberd AA, Lyra A, Ouwehand AC, et al. Intestinal microbiota is altered in patients with colon cancer and modified by probiotic intervention. BMJ Open Gastroenterol. 2017;4:e145.CrossRef Hibberd AA, Lyra A, Ouwehand AC, et al. Intestinal microbiota is altered in patients with colon cancer and modified by probiotic intervention. BMJ Open Gastroenterol. 2017;4:e145.CrossRef
4.
go back to reference Pushalkar S, Hundeyin M, Daley D, et al. The pancreatic cancer microbiome promotes oncogenesis by induction of innate and adaptive immune suppression. Cancer Discov. 2018;8:403–416.CrossRefPubMedPubMedCentral Pushalkar S, Hundeyin M, Daley D, et al. The pancreatic cancer microbiome promotes oncogenesis by induction of innate and adaptive immune suppression. Cancer Discov. 2018;8:403–416.CrossRefPubMedPubMedCentral
5.
go back to reference Zhao L, Zhang F, Ding X, et al. Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes. Science. 2018;359:1151–1156.CrossRefPubMed Zhao L, Zhang F, Ding X, et al. Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes. Science. 2018;359:1151–1156.CrossRefPubMed
6.
go back to reference Sampson TR, Debelius JW, Thron T, et al. Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson’s disease. Cell. 2016;167:1469–1480.CrossRefPubMedPubMedCentral Sampson TR, Debelius JW, Thron T, et al. Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson’s disease. Cell. 2016;167:1469–1480.CrossRefPubMedPubMedCentral
7.
go back to reference Ticinesi A, Milani C, Guerra A, et al. Understanding the gut-kidney axis in nephrolithiasis: an analysis of the gut microbiota composition and functionality of stone formers. Gut. 2018;2017:315–734. Ticinesi A, Milani C, Guerra A, et al. Understanding the gut-kidney axis in nephrolithiasis: an analysis of the gut microbiota composition and functionality of stone formers. Gut. 2018;2017:315–734.
9.
go back to reference Roy S, Trinchieri G. Microbiota: a key orchestrator of cancer therapy. Nat Rev Cancer. 2017;17:271–285.CrossRefPubMed Roy S, Trinchieri G. Microbiota: a key orchestrator of cancer therapy. Nat Rev Cancer. 2017;17:271–285.CrossRefPubMed
10.
go back to reference Xie YH, Gao QY, Cai GX, et al. Fecal Clostridium symbiosum for noninvasive detection of early and advanced colorectal cancer: test and validation studies. EBioMedicine. 2017;25:32–40.CrossRefPubMedPubMedCentral Xie YH, Gao QY, Cai GX, et al. Fecal Clostridium symbiosum for noninvasive detection of early and advanced colorectal cancer: test and validation studies. EBioMedicine. 2017;25:32–40.CrossRefPubMedPubMedCentral
11.
go back to reference Dai Z, Coker OO, Nakatsu G, et al. Multi-cohort analysis of colorectal cancer metagenome identified altered bacteria across populations and universal bacterial markers. Microbiome. 2018;6:70.CrossRefPubMedPubMedCentral Dai Z, Coker OO, Nakatsu G, et al. Multi-cohort analysis of colorectal cancer metagenome identified altered bacteria across populations and universal bacterial markers. Microbiome. 2018;6:70.CrossRefPubMedPubMedCentral
13.
go back to reference Li K, Dan Z, Gesang L, et al. Comparative analysis of gut microbiota of native Tibetan and Han populations living at different altitudes. PLoS ONE. 2016;11:e155863. Li K, Dan Z, Gesang L, et al. Comparative analysis of gut microbiota of native Tibetan and Han populations living at different altitudes. PLoS ONE. 2016;11:e155863.
14.
15.
go back to reference Costea PI, Hildebrand F, Arumugam M, et al. Enterotypes in the landscape of gut microbial community composition. Nat Microbiol. 2018;3:8–16.CrossRefPubMed Costea PI, Hildebrand F, Arumugam M, et al. Enterotypes in the landscape of gut microbial community composition. Nat Microbiol. 2018;3:8–16.CrossRefPubMed
16.
go back to reference Meehan CJ, Beiko RG. A phylogenomic view of ecological specialization in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biol Evol. 2014;6:703–713.CrossRefPubMedPubMedCentral Meehan CJ, Beiko RG. A phylogenomic view of ecological specialization in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biol Evol. 2014;6:703–713.CrossRefPubMedPubMedCentral
17.
go back to reference Zhou L, Zhang M, Wang Y, et al. Faecalibacterium prausnitzii produces butyrate to maintain Th17/Treg balance and to ameliorate colorectal colitis by inhibiting histone deacetylase 1. Inflamm Bowel Dis. 2018;12:S110–S111. Zhou L, Zhang M, Wang Y, et al. Faecalibacterium prausnitzii produces butyrate to maintain Th17/Treg balance and to ameliorate colorectal colitis by inhibiting histone deacetylase 1. Inflamm Bowel Dis. 2018;12:S110–S111.
18.
go back to reference McIntyre A, Gibson PR, Young GP. Butyrate production from dietary fibre and protection against large bowel cancer in a rat model. Gut. 1993;34:386–391.CrossRefPubMedPubMedCentral McIntyre A, Gibson PR, Young GP. Butyrate production from dietary fibre and protection against large bowel cancer in a rat model. Gut. 1993;34:386–391.CrossRefPubMedPubMedCentral
19.
go back to reference Roy MJ, Dionne S, Marx G, et al. In vitro studies on the inhibition of colon cancer by butyrate and carnitine. Nutrition. 2009;25:1193–1201.CrossRefPubMed Roy MJ, Dionne S, Marx G, et al. In vitro studies on the inhibition of colon cancer by butyrate and carnitine. Nutrition. 2009;25:1193–1201.CrossRefPubMed
20.
go back to reference Perrin P, Cassagnau E, Burg C, et al. An interleukin 2/sodium butyrate combination as immunotherapy for rat colon cancer peritoneal carcinomatosis. Gastroenterology. 1994;107:1697–1708.CrossRefPubMed Perrin P, Cassagnau E, Burg C, et al. An interleukin 2/sodium butyrate combination as immunotherapy for rat colon cancer peritoneal carcinomatosis. Gastroenterology. 1994;107:1697–1708.CrossRefPubMed
21.
go back to reference Berry D, Reinisch W. Intestinal microbiota: a source of novel biomarkers in inflammatory bowel diseases? Best Pract Res Clin Gastroenterol. 2013;27:47–58.CrossRefPubMed Berry D, Reinisch W. Intestinal microbiota: a source of novel biomarkers in inflammatory bowel diseases? Best Pract Res Clin Gastroenterol. 2013;27:47–58.CrossRefPubMed
22.
go back to reference Dejea CM, Fathi P, Craig JM, et al. Patients with familial adenomatous polyposis harbor colonic biofilms containing tumorigenic bacteria. Science. 2018;359:592–597.CrossRefPubMedPubMedCentral Dejea CM, Fathi P, Craig JM, et al. Patients with familial adenomatous polyposis harbor colonic biofilms containing tumorigenic bacteria. Science. 2018;359:592–597.CrossRefPubMedPubMedCentral
23.
go back to reference Wang L, Zhou J, Xin Y, et al. Bacterial overgrowth and diversification of microbiota in gastric cancer. Eur J Gastroenterol Hepatol. 2016;28:261–266.CrossRefPubMedPubMedCentral Wang L, Zhou J, Xin Y, et al. Bacterial overgrowth and diversification of microbiota in gastric cancer. Eur J Gastroenterol Hepatol. 2016;28:261–266.CrossRefPubMedPubMedCentral
24.
go back to reference Aviles-Jimenez F, Vazquez-Jimenez F, Medrano-Guzman R, Mantilla A, Torres J. Stomach microbiota composition varies between patients with non-atrophic gastritis and patients with intestinal type of gastric cancer. Sci Rep. 2014;4:4202.CrossRefPubMedPubMedCentral Aviles-Jimenez F, Vazquez-Jimenez F, Medrano-Guzman R, Mantilla A, Torres J. Stomach microbiota composition varies between patients with non-atrophic gastritis and patients with intestinal type of gastric cancer. Sci Rep. 2014;4:4202.CrossRefPubMedPubMedCentral
25.
go back to reference Cuevas-Ramos G, Petit CR, Marcq I, Boury M, Oswald E, Nougayrede JP. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci USA. 2010;107:11537–11542.CrossRefPubMedPubMedCentral Cuevas-Ramos G, Petit CR, Marcq I, Boury M, Oswald E, Nougayrede JP. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci USA. 2010;107:11537–11542.CrossRefPubMedPubMedCentral
26.
go back to reference Kaur CP, Vadivelu J, Chandramathi S. Impact of Klebsiella pneumoniae in lower gastrointestinal tract diseases. J Dig Dis. 2018;19:262–271.CrossRefPubMed Kaur CP, Vadivelu J, Chandramathi S. Impact of Klebsiella pneumoniae in lower gastrointestinal tract diseases. J Dig Dis. 2018;19:262–271.CrossRefPubMed
27.
go back to reference Jo HJ, Kim J, Kim N, et al. Analysis of gastric microbiota by pyrosequencing: minor role of bacteria other than Helicobacter pylori in the gastric carcinogenesis. Helicobacter. 2016;21:364–374.CrossRefPubMed Jo HJ, Kim J, Kim N, et al. Analysis of gastric microbiota by pyrosequencing: minor role of bacteria other than Helicobacter pylori in the gastric carcinogenesis. Helicobacter. 2016;21:364–374.CrossRefPubMed
28.
go back to reference Coker OO, Dai Z, Nie Y, et al. Mucosal microbiome dysbiosis in gastric carcinogenesis. Gut. 2018;67:1024–1032.CrossRefPubMed Coker OO, Dai Z, Nie Y, et al. Mucosal microbiome dysbiosis in gastric carcinogenesis. Gut. 2018;67:1024–1032.CrossRefPubMed
29.
go back to reference Antharam VC, Li EC, Ishmael A, et al. Intestinal dysbiosis and depletion of butyrogenic bacteria in Clostridium difficile infection and nosocomial diarrhea. J Clin Microbiol. 2013;51:2884–2892.CrossRefPubMedPubMedCentral Antharam VC, Li EC, Ishmael A, et al. Intestinal dysbiosis and depletion of butyrogenic bacteria in Clostridium difficile infection and nosocomial diarrhea. J Clin Microbiol. 2013;51:2884–2892.CrossRefPubMedPubMedCentral
30.
go back to reference Jackson MA, Goodrich JK, Maxan ME, et al. Proton pump inhibitors alter the composition of the gut microbiota. Gut. 2016;65:749–756.CrossRefPubMed Jackson MA, Goodrich JK, Maxan ME, et al. Proton pump inhibitors alter the composition of the gut microbiota. Gut. 2016;65:749–756.CrossRefPubMed
31.
go back to reference Imhann F, Bonder MJ, Vich VA, et al. Proton pump inhibitors affect the gut microbiome. Gut. 2016;65:740–748.CrossRefPubMed Imhann F, Bonder MJ, Vich VA, et al. Proton pump inhibitors affect the gut microbiome. Gut. 2016;65:740–748.CrossRefPubMed
32.
go back to reference Gao F, Li M, Liu Y, Gao C, Wen S, Tang L. Intestinal dysbacteriosis induces changes of T lymphocyte subpopulations in Peyer’s patches of mice and orients the immune response towards humoral immunity. Gut Pathog. 2012;4:19.CrossRefPubMedPubMedCentral Gao F, Li M, Liu Y, Gao C, Wen S, Tang L. Intestinal dysbacteriosis induces changes of T lymphocyte subpopulations in Peyer’s patches of mice and orients the immune response towards humoral immunity. Gut Pathog. 2012;4:19.CrossRefPubMedPubMedCentral
Metadata
Title
Intestinal Microbiota Is Altered in Patients with Gastric Cancer from Shanxi Province, China
Authors
Yu-feng Qi
Jun-ning Sun
Lai-feng Ren
Xue-ling Cao
Jian-hong Dong
Kai Tao
Xue-mei Guan
Ya-ni Cui
Wen Su
Publication date
01-05-2019
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 5/2019
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-018-5411-y

Other articles of this Issue 5/2019

Digestive Diseases and Sciences 5/2019 Go to the issue