Advertisement

Journal of Gastroenterology

, Volume 54, Issue 1, pp 53–63 | Cite as

Differences in gut microbiota associated with age, sex, and stool consistency in healthy Japanese subjects

  • Tomohisa Takagi
  • Yuji Naito
  • Ryo Inoue
  • Saori Kashiwagi
  • Kazuhiko Uchiyama
  • Katsura Mizushima
  • Saeko Tsuchiya
  • Osamu Dohi
  • Naohisa Yoshida
  • Kazuhiro Kamada
  • Takeshi Ishikawa
  • Osamu Handa
  • Hideyuki Konishi
  • Kayo Okuda
  • Yoshimasa Tsujimoto
  • Hiromu Ohnogi
  • Yoshito Itoh
Original Article—Alimentary Tract

Abstract

Background

Human gut microbiota is involved in host health and disease development. Investigations of age-related and sex-related alterations in gut microbiota are limited, and the association between stool consistency and gut microbiota has not been fully investigated. We investigated gut microbiota differences related to age, sex, and stool consistency in healthy Japanese subjects.

Methods

Two-hundred and seventy-seven healthy Japanese subjects aged 20–89 years were enrolled. Fecal samples were obtained to analyze the gut microbiome. We evaluated the association between stool consistency [Bristol stool scale (BSS)] and gut microbiota.

Results

Although there were significant differences in the microbial structure between males and females, the α-diversity of gut microbiota showed no difference between males and females or among age groups. There were significant increases in genera Prevotella, Megamonas, Fusobacterium, and Megasphaera and Bifidobacterium, Ruminococcus, and Akkermansia in males and females, respectively. The ratio of hard stools (BSS types 1 and 2) was higher in females; the ratio of loose stools (BSS type 6) was higher in males. No younger male had BSS type 1 or type 2. Fusobacterium in males was significantly higher in the loose consistency group, and Oscillospira was significantly higher in the hard consistency group in males; Campylobacter, SMB53, and Turicibacter were significantly higher in the hard consistency group in females.

Conclusions

Several changes in gut microbiota were associated with age and sex. Stool consistency and gut microbiota associations emphasized the importance of stool consistency assessments to understand intestinal function.

Keywords

Gut microbiota 16S rRNA Bristol stool scale 

Notes

Acknowledgements

This work was supported by grants-in-aid for Scientific Research (KAKENHI) to Tomohisa Takagi (grant no. 16K09322) and Yuji Naito (grant no. 16H05289) from the Japan Society for the Promotion of Science and by the Grant of Industry-Academia-Government Collaboration of “Field for Knowledge Integration and Innovation” (FKII) to Yuji Naito (no. 28020006) from the Ministry of Agriculture, Forestry, and Fisheries of Japan. This work was performed in collaboration with Takara Bio Inc.

Author contributions

TT, NY, IR, and KS conceived the experiments; TT, UK, DO, YN, KK, IT, HO, and KH collected feces; OK, TY, and OH performed analyses of fecal bacteria; IR, KS, MK, and TA analyzed data; and TT, NY, and IY were involved in editing the manuscript. All authors discussed the results and commented on the manuscript.

Compliance with ethical standards

Conflict of interest

Dr. Tomohisa Takagi received lecture fees from Mochida Pharm. Co. Ltd. and Miysubishi Tanabe Pharma Co. Dr. Yuji Naito received scholarship funds from EA Pharma. Co. Ltd. and collaboration research funds from Fujifilm Medical Co., Ltd. and has been paid lecture fees by Janssen Pharma K.K., Mylan EPD Co., Takeda Pharma Co., Ltd., Mochida Pharm. Co., Ltd., EA Pharma Co., Ltd., Otsuka Pharma Co., Ltd., and Astellas Pharma Co., Ltd. Dr. Yoshito Itoh is affiliated with a department funded by donations from Nichinichi Pharmaceutical Co., Ltd. and has received research grants from Takeda Pharmaceutical Co., Ltd. and EA Pharma Co., Ltd. The other authors have no conflicts of interest to declare.

Supplementary material

535_2018_1488_MOESM1_ESM.xlsx (39 kb)
Supplementary material 1 (XLSX 40 kb)
535_2018_1488_MOESM2_ESM.pptx (12.6 mb)
Supplementary material 2 (PPTX 12940 kb)

References

  1. 1.
    Lynch SV, Pedersen O. The human intestinal microbiome in health and disease. N Engl J Med. 2016;375:2369–79.CrossRefGoogle Scholar
  2. 2.
    Clemente JC, Ursell LK, Parfrey LW, et al. The impact of the gut microbiota on human health: an integrative view. Cell. 2012;148:1258–70.CrossRefGoogle Scholar
  3. 3.
    Kedia S, Rampal R, Paul J, et al. Gut microbiome diversity in acute infective and chronic inflammatory gastrointestinal diseases in North India. J Gastroenterol. 2016;51:660–71.CrossRefGoogle Scholar
  4. 4.
    Ley RE, Turnbaugh PJ, Klein S, et al. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022–3.CrossRefGoogle Scholar
  5. 5.
    Vandeputte D, Falony G, Vieira-Silva S, et al. Stool consistency is strongly associated with gut microbiota richness and composition, enterotypes and bacterial growth rates. Gut. 2016;65:57–62.CrossRefGoogle Scholar
  6. 6.
    Tigchelaar EF, Bonder MJ, Jankipersadsing SA, et al. Gut microbiota composition associated with stool consistency. Gut. 2016;65:540–2.CrossRefGoogle Scholar
  7. 7.
    Hadizadeh F, Walter S, Belheouane M, et al. Stool frequency is associated with gut microbiota composition. Gut. 2017;66:559–60.CrossRefGoogle Scholar
  8. 8.
    Longstreth GF, Thompson WG, Chey WD, et al. Functional bowel disorders. Gastroenterology. 2006;130:1480–91.CrossRefGoogle Scholar
  9. 9.
    Degen LP, Phillips SF. How well does stool form reflect colonic transit? Gut. 1996;39:109–13.CrossRefGoogle Scholar
  10. 10.
    Consortium THMP. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207–14.CrossRefGoogle Scholar
  11. 11.
    Arumugam M, Raes J, Pelletier E, et al. Enterotypes of the human gut microbiome. Nature. 2011;473:174–80.CrossRefGoogle Scholar
  12. 12.
    Nishijima S, Suda W, Oshima K, Kim SW, Hirose Y, Morita H, et al. The gut microbiome of healthy Japanese and its microbial and functional uniqueness. DNA Res. 2016;23:125–33.CrossRefGoogle Scholar
  13. 13.
    Nakayama J, Watanabe K, Jiang J, et al. Diversity in gut bacterial community of school-age children in Asia. Sci Rep. 2015;5:8397.CrossRefGoogle Scholar
  14. 14.
    Heaton KW, Radvan J, Cripps H, et al. Defecation frequency and timing, and stool form in the general population: a prospective study. Gut. 1992;33:818–24.CrossRefGoogle Scholar
  15. 15.
    Inoue R, Ohue-Kitano R, Tsukahara T, et al. Prediction of functional profiles of gut microbiota from 16S rRNA metagenomic data provides a more robust evaluation of gut dysbiosis occurring in Japanese type 2 diabetic patients. J Clin Biochem Nutr. 2017;61:217–21.CrossRefGoogle Scholar
  16. 16.
    Nishino K, Nishida A, Inoue R, et al. Analysis of endoscopic brush samples identified mucosa-associated dysbiosis in inflammatory bowel disease. J Gastroenterol. 2018;53:95–106.CrossRefGoogle Scholar
  17. 17.
    Takagi T, Naito Y, Inoue R, et al. The influence of long-term use of proton pump inhibitors on the gut microbiota: an age-sex-matched case-control study. J Clin Biochem Nutr. 2018;62:100–5.CrossRefGoogle Scholar
  18. 18.
    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.CrossRefGoogle Scholar
  19. 19.
    Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics (Oxford, England). 2010;26:2460–1.CrossRefGoogle Scholar
  20. 20.
    Edgar RC, Haas BJ, Clemente JC, et al. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics (Oxford, England). 2011;27:2194–200.CrossRefGoogle Scholar
  21. 21.
    Koliada A, Syzenko G, Moseiko V, et al. Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population. BMC Microbiol. 2017;17:120.CrossRefGoogle Scholar
  22. 22.
    Ley RE, Backhed F, Turnbaugh P, et al. Obesity alters gut microbial ecology. Proc Natl Acad Sci USA. 2005;102:11070–5.CrossRefGoogle Scholar
  23. 23.
    Mathur R, Barlow GM. Obesity and the microbiome. Expert Rev Gastroenterol Hepatol. 2015;9:1087–99.CrossRefGoogle Scholar
  24. 24.
    Ignacio A, Fernandes MR, Rodrigues VA, et al. Correlation between body mass index and faecal microbiota from children. Clin Microbiol Infect. 2016;22:258.e1–e8.CrossRefGoogle Scholar
  25. 25.
    Schwiertz A, Taras D, Schafer K, et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring, Md). 2010;18:190–5.CrossRefGoogle Scholar
  26. 26.
    Odamaki T, Kato K, Sugahara H, et al. Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiol. 2016;16:90.CrossRefGoogle Scholar
  27. 27.
    Wang JJ, Wang J, Pang XY, et al. Sex differences in colonization of gut microbiota from a man with short-term vegetarian and inulin-supplemented diet in germ-free mice. Sci Rep. 2016;6:36137.CrossRefGoogle Scholar
  28. 28.
    Markle JG, Frank DN, Mortin-Toth S, et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science. 2013;339:1084–8.CrossRefGoogle Scholar
  29. 29.
    Org E, Mehrabian M, Parks BW, et al. Sex differences and hormonal effects on gut microbiota composition in mice. Gut Microbes. 2016;7:313–22.CrossRefGoogle Scholar
  30. 30.
    Fransen F, van Beek AA, Borghuis T, et al. The impact of gut microbiota on gender-specific differences in immunity. Front Immunol. 2017;8:754.CrossRefGoogle Scholar
  31. 31.
    Yatsunenko T, Rey FE, Manary MJ, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222–7.CrossRefGoogle Scholar
  32. 32.
    Sonnenburg JL, Backhed F. Diet-microbiota interactions as moderators of human metabolism. Nature. 2016;535:56–64.CrossRefGoogle Scholar
  33. 33.
    Kasai C, Sugimoto K, Moritani I, et al. Comparison of the gut microbiota composition between obese and non-obese individuals in a Japanese population, as analyzed by terminal restriction fragment length polymorphism and next-generation sequencing. BMC Gastroenterol. 2015;15:100.CrossRefGoogle Scholar
  34. 34.
    Lewis SJ, Heaton KW. Stool form scale as a useful guide to intestinal transit time. Scand J Gastroenterol. 1997;32:920–4.CrossRefGoogle Scholar
  35. 35.
    Tian H, Ge X, Nie Y, et al. Fecal microbiota transplantation in patients with slow-transit constipation: a randomized, clinical trial. PLoS One. 2017;12:e0171308.CrossRefGoogle Scholar
  36. 36.
    Halkjaer SI, Boolsen AW, Gunther S, et al. Can fecal microbiota transplantation cure irritable bowel syndrome? World J Gastroenterol. 2017;23:4112–20.CrossRefGoogle Scholar
  37. 37.
    Abadi ATB. Fecal microbiota transplantation against irritable bowel syndrome? Rigorous randomized clinical trials are required. World J Gastrointest Pharmacol Ther. 2017;8:208–9.CrossRefGoogle Scholar
  38. 38.
    Mizuno S, Masaoka T, Naganuma M, et al. Bifidobacterium-rich fecal donor may be a positive predictor for successful fecal microbiota transplantation in patients with irritable bowel syndrome. Digestion. 2017;96:29–38.CrossRefGoogle Scholar
  39. 39.
    Agrawal A, Houghton LA, Morris J, et al. Clinical trial: the effects of a fermented milk product containing Bifidobacterium lactis DN-173 010 on abdominal distension and gastrointestinal transit in irritable bowel syndrome with constipation. Aliment Pharmacol Ther. 2009;29:104–14.CrossRefGoogle Scholar
  40. 40.
    Kim HJ, Vazquez Roque MI, Camilleri M, et al. A randomized controlled trial of a probiotic combination VSL# 3 and placebo in irritable bowel syndrome with bloating. Neurogastroenterol Motil. 2005;17:687–96.CrossRefGoogle Scholar

Copyright information

© Japanese Society of Gastroenterology 2018

Authors and Affiliations

  • Tomohisa Takagi
    • 1
    • 2
  • Yuji Naito
    • 1
  • Ryo Inoue
    • 3
  • Saori Kashiwagi
    • 1
  • Kazuhiko Uchiyama
    • 1
  • Katsura Mizushima
    • 1
  • Saeko Tsuchiya
    • 1
  • Osamu Dohi
    • 1
  • Naohisa Yoshida
    • 1
  • Kazuhiro Kamada
    • 1
  • Takeshi Ishikawa
    • 1
  • Osamu Handa
    • 1
  • Hideyuki Konishi
    • 1
  • Kayo Okuda
    • 4
  • Yoshimasa Tsujimoto
    • 4
  • Hiromu Ohnogi
    • 4
  • Yoshito Itoh
    • 1
  1. 1.Molecular Gastroenterology and Hepatology, Graduate School of Medical ScienceKyoto Prefectural University of MedicineKyotoJapan
  2. 2.Department for Medical Innovation and Translational Medical Science, Graduate School of Medical ScienceKyoto Prefectural University of MedicineKyotoJapan
  3. 3.Laboratory of Animal ScienceKyoto Prefectural UniversityKyotoJapan
  4. 4.Takara Bio Inc.ShigaJapan

Personalised recommendations