Differences in intestinal microbiota profiling after upper and lower gastrointestinal surgery.


Journal

Journal of the Chinese Medical Association : JCMA
ISSN: 1728-7731
Titre abrégé: J Chin Med Assoc
Pays: Netherlands
ID NLM: 101174817

Informations de publication

Date de publication:
01 04 2021
Historique:
pubmed: 5 3 2021
medline: 18 12 2021
entrez: 4 3 2021
Statut: ppublish

Résumé

We aimed to investigate the long-term effects of metabolic profiles and microbiota status in patients after upper gastrointestinal (GI) surgery and lower GI surgery and compared them with a control group. In this cross-sectional study, we analyzed the occurrence of metabolic syndrome (MS) in 10 patients who underwent curative total gastrectomy with Roux-en-Y esophagojejunostomy (RYEJ) anastomosis, 11 patients who underwent curative partial colectomy with right hemicolectomy (RH), and 33 age- and sex-matched controls. Fecal samples were also analyzed by a next-generation sequencing method. Compared with the control group, the occurrence of MS was significantly lower among patients who underwent total gastrectomy with RYEJ than the controls over the long-term follow-up (>8 years; p < 0.05). Patients who received RH only had a trend of higher serum fasting glucose (p = 0.10). The diversity of the gut microbiota significantly decreased after RH in comparison with the control group and RYEJ group, respectively (p < 0.05). Principal component analysis revealed significant differences between the control, RYEJ, and RH groups (p < 0.001). At the genus level, the ratio of Prevotella to Bacteroides (P/B) was significantly higher in the RYEJ group than in the control group, whereas the P/B ratio was significantly lower in the RH group than in the control group (p < 0.05). Early gastric cancer patients who received total gastrectomy with RYEJ had a lower occurrence of MS than the controls, while early colorectal cancer patients who received RH were associated with a higher serum fasting glucose than the controls during long-term follow-up. In parallel with the metabolic differences, the P/B ratio was also significantly altered in patients after upper and lower GI surgery.

Sections du résumé

BACKGROUND
We aimed to investigate the long-term effects of metabolic profiles and microbiota status in patients after upper gastrointestinal (GI) surgery and lower GI surgery and compared them with a control group.
METHODS
In this cross-sectional study, we analyzed the occurrence of metabolic syndrome (MS) in 10 patients who underwent curative total gastrectomy with Roux-en-Y esophagojejunostomy (RYEJ) anastomosis, 11 patients who underwent curative partial colectomy with right hemicolectomy (RH), and 33 age- and sex-matched controls. Fecal samples were also analyzed by a next-generation sequencing method.
RESULTS
Compared with the control group, the occurrence of MS was significantly lower among patients who underwent total gastrectomy with RYEJ than the controls over the long-term follow-up (>8 years; p < 0.05). Patients who received RH only had a trend of higher serum fasting glucose (p = 0.10). The diversity of the gut microbiota significantly decreased after RH in comparison with the control group and RYEJ group, respectively (p < 0.05). Principal component analysis revealed significant differences between the control, RYEJ, and RH groups (p < 0.001). At the genus level, the ratio of Prevotella to Bacteroides (P/B) was significantly higher in the RYEJ group than in the control group, whereas the P/B ratio was significantly lower in the RH group than in the control group (p < 0.05).
CONCLUSION
Early gastric cancer patients who received total gastrectomy with RYEJ had a lower occurrence of MS than the controls, while early colorectal cancer patients who received RH were associated with a higher serum fasting glucose than the controls during long-term follow-up. In parallel with the metabolic differences, the P/B ratio was also significantly altered in patients after upper and lower GI surgery.

Identifiants

pubmed: 33660622
doi: 10.1097/JCMA.0000000000000510
pii: 02118582-202104000-00004
doi:

Types de publication

Comparative Study Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

354-360

Informations de copyright

Copyright © 2021, the Chinese Medical Association.

Déclaration de conflit d'intérêts

Conflicts of interest: The authors declare that they have no conflicts of interest related to the subject matter or materials discussed in this article.

Références

Fournel A, Marlin A, Abot A, Pasquio C, Cirillo C, Cani PD, et al. Glucosensing in the gastrointestinal tract: impact on glucose metabolism. Am J Physiol Gastrointest Liver Physiol. 2016; 310:G645–58
Sheng B, Truong K, Spitler H, Zhang L, Tong X, Chen L. The long-term effects of bariatric surgery on type 2 diabetes remission, microvascular and macrovascular complications, and mortality: a systematic review and meta-analysis. Obes Surg. 2017; 27:2724–32
Tremaroli V, Karlsson F, Werling M, Ståhlman M, Kovatcheva-Datchary P, Olbers T, et al. Roux-en-Y gastric bypass and vertical banded gastroplasty induce long-term changes on the human gut microbiome contributing to fat mass regulation. Cell Metab. 2015; 22:228–38
Lin XH, Huang KH, Chuang WH, Luo JC, Lin CC, Ting PH, et al. The long term effect of metabolic profile and microbiota status in early gastric cancer patients after subtotal gastrectomy. PLoS One. 2018; 13:e0206930
Palnaes Hansen C, Andreasen JJ, Holst JJ. The release of gastric inhibitory peptide, glucagon-like peptide-I, and insulin after oral glucose test in colectomized subjects. Scand J Gastroenterol. 1997; 32:473–7
Robertson MD, Bickerton AS, Dennis AL, Vidal H, Jewell DP, Frayn KN. Enhanced metabolic cycling in subjects after colonic resection for ulcerative colitis. J Clin Endocrinol Metab. 2005; 90:2747–54
Ussar S, Griffin NW, Bezy O, Fujisaka S, Vienberg S, Softic S, et al. Interactions between gut microbiota, host genetics and diet modulate the predisposition to obesity and metabolic syndrome. Cell Metab. 2015; 22:516–30
Japanese Gastric Cancer AssociationJapanese classification of gastric carcinoma - 2nd. english edition. Gastric Cancer. 1998; 1:10–24
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010; 7:335–6
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: high-resolution sample inference from illumina amplicon data. Nat Methods. 2016; 13:581–3
Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016; 4:e2584
Goecks J, Nekrutenko A, Taylor J. Galaxy TeamGalaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol. 2010; 11:R86
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011; 12:R60
Medhus AW, Bjørnland K, Emblem R, Haug E, Husebye E. Are patients with Hirschsprung’s disease prediabetic? Metabolism. 2001; 50:1389–90
Lin XH, Jiang JK, Luo JC, Lin CC, Ting PH, Yang UC, et al. The long term microbiota and metabolic status in patients with colorectal cancer after curative colon surgery. PLoS One. 2019; 14:e0218436
Furet JP, Kong LC, Tap J, Poitou C, Basdevant A, Bouillot JL, et al. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes. 2010; 59:3049–57
Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A. 2009; 106:2365–70
Li JV, Ashrafian H, Bueter M, Kinross J, Sands C, le Roux CW, et al. Metabolic surgery profoundly influences gut microbial-host metabolic cross-talk. Gut. 2011; 60:1214–23
Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One. 2010; 5:e9085
Matsha TE, Prince Y, Davids S, Chikte U, Erasmus RT, Kengne AP, et al. Oral microbiome signatures in diabetes mellitus and periodontal disease. J Dent Res. 2020; 99:658–65
Minty M, Canceil T, Serino M, Burcelin R, Tercé F, Blasco-Baque V. Oral microbiota-induced periodontitis: a new risk factor of metabolic diseases. Rev Endocr Metab Disord. 2019; 20:449–59
Sakalauskiene J, Kubilius R, Gleiznys A, Vitkauskiene A, Ivanauskiene E, Šaferis V. Relationship of clinical and microbiological variables in patients with type 1 diabetes mellitus and periodontitis. Med Sci Monit. 2014; 20:1871–7
Mashima I, Nakazawa F. The interaction between Streptococcus spp. and Veillonella tobetsuensis in the early stages of oral biofilm formation. J Bacteriol. 2015; 197:2104–11
Hjorth MF, Blædel T, Bendtsen LQ, Lorenzen JK, Holm JB, Kiilerich P, et al. Prevotella-to-Bacteroides ratio predicts body weight and fat loss success on 24-week diets varying in macronutrient composition and dietary fiber: results from a post-hoc analysis. Int J Obes (Lond). 2019; 43:149–57
Lim MY, Rho M, Song YM, Lee K, Sung J, Ko G. Stability of gut enterotypes in Korean monozygotic twins and their association with biomarkers and diet. Sci Rep. 2014; 4:7348
Roager HM, Licht TR, Poulsen SK, Larsen TM, Bahl MI. Microbial enterotypes, inferred by the Prevotella-to-Bacteroides ratio, remained stable during a 6-month randomized controlled diet intervention with the new Nordic diet. Appl Environ Microbiol. 2014; 80:1142–9
Hjorth MF, Roager HM, Larsen TM, Poulsen SK, Licht TR, Bahl MI, et al. Pre-treatment microbial Prevotella-to-Bacteroides ratio, determines body fat loss success during a 6-month randomized controlled diet intervention. Int J Obes (Lond). 2018; 42:580–3
Guyton K, Alverdy JC. The gut microbiota and gastrointestinal surgery. Nat Rev Gastroenterol Hepatol. 2017; 14:43–54
Kovatcheva-Datchary P, Nilsson A, Akrami R, Lee YS, De Vadder F, Arora T, et al. Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of Prevotella. Cell Metab. 2015; 22:971–82
Robertson MD, Livesey G, Hampton SM, Mathers JC. Evidence for altered control of glucose disposal after total colectomy. Br J Nutr. 2000; 84:813–9
Scheppach W, Pomare EW, Elia M, Cummings JH. The contribution of the large intestine to blood acetate in man. Clin Sci (Lond). 1991; 80:177–82

Auteurs

Xi-Hsuan Lin (XH)

Department of Medicine, National Yang Ming Chiao Tung University Hospital, Yilan, Taiwan, ROC.
Department of Medicine, National Yang Ming Chiao Tung University, School of Medicine, Taipei, Taiwan, ROC.

Ueng-Cheng Yang (UC)

School of Medicine, Institute of Biomedical Informatics, National Yang Ming Chiao Tung University, Taipei, Taiwan, ROC.

Jiing-Chyuan Luo (JC)

Department of Medicine, National Yang Ming Chiao Tung University, School of Medicine, Taipei, Taiwan, ROC.
Division of Gastroenterology and Hepatology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan, ROC.
Department of Medicine, Keelung Hospital, Ministry of Health Welfare, Keelung, Taiwan, ROC.

Tien-En Chang (TE)

Department of Medicine, National Yang Ming Chiao Tung University, School of Medicine, Taipei, Taiwan, ROC.
Division of Gastroenterology and Hepatology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan, ROC.

Hung-Hsin Lin (HH)

Department of Medicine, National Yang Ming Chiao Tung University, School of Medicine, Taipei, Taiwan, ROC.
Division of Colon and Rectal Surgery, Taipei Veterans General Hospital, Taipei, Taiwan, ROC.

Chi-Wei Huang (CW)

School of Medicine, Institute of Biomedical Informatics, National Yang Ming Chiao Tung University, Taipei, Taiwan, ROC.

Jen-Jie Chiou (JJ)

School of Medicine, Institute of Biomedical Informatics, National Yang Ming Chiao Tung University, Taipei, Taiwan, ROC.

Wen-Liang Fang (WL)

Department of Medicine, National Yang Ming Chiao Tung University, School of Medicine, Taipei, Taiwan, ROC.
Division of General Surgery, Department of Surgery, Taipei Veterans General Hospital, Taipei, Taiwan, ROC.

Kuo-Hung Huang (KH)

Department of Medicine, National Yang Ming Chiao Tung University, School of Medicine, Taipei, Taiwan, ROC.
Division of General Surgery, Department of Surgery, Taipei Veterans General Hospital, Taipei, Taiwan, ROC.

Yi-Hsiang Huang (YH)

Department of Medicine, National Yang Ming Chiao Tung University, School of Medicine, Taipei, Taiwan, ROC.
Division of Gastroenterology and Hepatology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan, ROC.

Ming-Chih Hou (MC)

Department of Medicine, National Yang Ming Chiao Tung University, School of Medicine, Taipei, Taiwan, ROC.
Division of Gastroenterology and Hepatology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan, ROC.

Fa-Yauh Lee (FY)

Department of Medicine, National Yang Ming Chiao Tung University, School of Medicine, Taipei, Taiwan, ROC.
Division of Gastroenterology and Hepatology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan, ROC.

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