Age-related changes in production of short-chain fatty acids by gut microbiome in patients without gastroenterological diseases

Cover Page

Cite item

Abstract

Rationale: Multiple biological effects of short chain fatty acids (SCFA) and the possibility to modify their composition by probiotics and prebiotics is in the focus of attention of researchers and clinicians. However, big studies with assessment of the whole spectrum of SCFA produced by gut microbiome and calculated indexes of their relative content are lacking.

Aim: To determine concentrations and ratios of fecal SCFA (functional activity of the gut microbiome) depending on the age of patients without gastrointestinal disorders.

Materials and methods: SCFA fecal concentrations were measured by gas liquid chromatography in 6836 patients aged from 1 month to 85 years without any functional or chronic gastrointestinal pathology, infectious diseases and/or obesity. The time periods with homogenous values of the parameters were determined by identification of constant trends of their means (medians) with 1-month accuracy in children below 5 years of age and with 1-year accuracy in the patients above 1 years of age. The results obtained for the chosen time intervals were compared with Mann-Whitney's test at 95% significance level (p < 0.05).

Results: We performed descriptive statistics for absolute and relative content of SCFA and their structural indexes. It was shown that the parameters characterizing functional activity of gut microbiome have different critical stages in their age-related changes. For each parameter, 2 or 3 stages of changes were identified that occurred at early age, mainly before the age of two. The final SCFA structure was stable by 2 years and 5 months of age. Total SCFA levels reached those typical for adults by the age of 12. The structural index was most sensitive to integrated changes of the microbiome structure.

Conclusion: Age-related characteristics of gut microbiome should be taken into account when performing clinical studies on effectiveness of therapeutic interventions and assessing the parameters in a given patient.

About the authors

A. M. Zatevalov

Gabrichevsky Moscow Research Institute of Epidemiology and Microbiology

Author for correspondence.
Email: 89057149114@mail.ru

Alexander M. Zatevalov – PhD, Doctor of Biol. Sci., Chief Research Fellow, Laboratory of Diagnosis and Prevention of Infectious Diseases.

11–5 Detskaya ul., Zheleznodorozhny town, Moscow Region, 143985, Russian Federation, tel.: +7 (905) 714 91 14

Russian Federation

E. P. Selkova

Gabrichevsky Moscow Research Institute of Epidemiology and Microbiology

Email: fake@neicon.ru

Eugenia P. Selkova – MD, PhD, Head of the Laboratory of Diagnosis and Prevention of Infectious Diseases, Chief Research Fellow.

10 Admirala Makarova ul., Moscow, 125212

Russian Federation

N. V. Gudova

Gabrichevsky Moscow Research Institute of Epidemiology and Microbiology

Email: fake@neicon.ru

Natalia V. Gudova – Research Fellow, Laboratory of Diagnosis and Prevention of Infectious Diseases.

10 Admirala Makarova ul., Moscow, 125212

Russian Federation

A. S. Oganesyan

Gabrichevsky Moscow Research Institute of Epidemiology and Microbiology

Email: fake@neicon.ru

Arpine S. Oganesyan – Research Fellow, Laboratory of Diagnosis and Prevention of Infectious Diseases.

10 Admirala Makarova ul., Moscow, 125212

Russian Federation

References

  1. Havenaar R. Intestinal health functions of colonic microbial metabolites: a review. Benef Microbes. 2011;2(2): 103–14. doi: 10.3920/BM2011.0003.
  2. Tan J, McKenzie C, Potamitis M, Thorburn AN, Mackay CR, Macia L. The role of short-chain fatty acids in health and disease. Adv Immunol. 2014;121:91–119. doi: 10.1016/B978-0-12800100-4.00003-9.
  3. Cavaliere M, Feng S, Soyer OS, Jiménez JI. Cooperation in microbial communities and their biotechnological applications. Environ Microbiol. 2017;19(8): 2949–63. doi: 10.1111/14622920.13767.
  4. Li M, van Esch BCAM, Henricks PAJ, Garssen J, Folkerts G. Time and concentration dependent effects of short chain fatty acids on lipopolysaccharide- or tumor necrosis factor α-induced endothelial activation. Front Pharmacol. 2018;9:233. doi: 10.3389/fphar.2018.00233.
  5. Sivaprakasam S, Bhutia YD, Yang S, Ganapathy V. Short-chain fatty acid transporters: role in colonic homeostasis. Compr Physiol. 2017;8(1): 299–314. doi: 10.1002/cphy.c170014.
  6. Sivaprakasam S, Prasad PD, Singh N. Benefits of short-chain fatty acids and their receptors in inflammation and carcinogenesis. Pharmacol Ther. 2016;164:144–51. doi: 10.1016/j.pharmthera.2016.04.007.
  7. Bruce-Keller AJ, Salbaum JM, Berthoud HR. Harnessing gut microbes for mental health: getting from here to there. Biol Psychiatry. 2018;83(3): 214–23. doi: 10.1016/j.biopsych.2017.08.014.
  8. Berni Canani R, De Filippis F, Nocerino R, Laiola M, Paparo L, Calignano A, De Caro C, Coretti L, Chiariotti L, Gilbert JA, Ercolini D. Specific Signatures of the Gut Microbiota and Increased Levels of Butyrate in Children Treated with Fermented Cow's Milk Containing Heat-Killed Lactobacillus paracasei CBA L74. Appl Environ Microbiol. 2017;83(19). pii: e01206–17. doi: 10.1128/AEM.01206-17.
  9. Rastelli M, Knauf C, Cani PD. Gut microbes and health: a focus on the mechanisms linking microbes, obesity, and related disorders. Obesity (Silver Spring). 2018;26(5): 792–800. doi: 10.1002/oby.22175.
  10. Yoshioka K, Kakihana K, Doki N, Ohashi K. Gut microbiota and acute graft-versus-host disease. Pharmacol Res. 2017;122:90–5. doi: 10.1016/j.phrs.2017.05.028.
  11. Yamada T, Shimizu K, Ogura H, Asahara T, Nomoto K, Yamakawa K, Hamasaki T, Nakahori Y, Ohnishi M, Kuwagata Y, Shimazu T. Rapid and sustained long-term decrease of fecal shortchain fatty acids in critically ill patients with systemic inflammatory response syndrome. JPEN J Parenter Enteral Nutr. 2015;39(5): 569– 77. doi: 10.1177/0148607114529596.
  12. Guarino A, Canani RB. Probiotics in childhood diseases: from basic science to guidelines in 20 years of research and development. J Pediatr Gastroenterol Nutr. 2016;63 Suppl 1:S1–2. doi: 10.1097/MPG.0000000000001220.
  13. Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, Li Y, Xia Y, Xie H, Zhong H, Khan MT, Zhang J, Li J, Xiao L, Al-Aama J, Zhang D, Lee YS, Kotowska D, Colding C, Tremaroli V, Yin Y, Bergman S, Xu X, Madsen L, Kristiansen K, Dahlgren J, Wang J. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17(5): 690–703. doi: 10.1016/j.chom.2015.04.004.
  14. Bridgman SL, Azad MB, Field CJ, Haqq AM, Becker AB, Mandhane PJ, Subbarao P, Turvey SE, Sears MR, Scott JA, Wishart DS, Kozyrskyj AL; CHILD Study Investigators. Fecal Short-Chain Fatty Acid Variations by Breastfeeding Status in Infants at 4 Months: Differences in Relative versus Absolute Concentrations. Front Nutr. 2017;4:11. doi: 10.3389/fnut.2017.00011.
  15. Martin FP, Moco S, Montoliu I, Collino S, Da Silva L, Rezzi S, Prieto R, Kussmann M, Inostroza J, Steenhout P. Impact of breast-feeding and high- and low-protein formula on the metabolism and growth of infants from overweight and obese mothers. Pediatr Res. 2014;75(4): 535–43. doi: 10.1038/pr.2013.250.
  16. Shenderov BA. Probiotic (symbiotic) bacterial languages. Anaerobe. 2011;17(6): 490–5. doi: 10.1016/j.anaerobe.2011.05.009.
  17. Ардатская МД, Дубинин АВ, Минушкин ОН. Дисбактериоз кишечника: современные аспекты изучения проблемы, принципы диагностики и лечения. Терапевтический архив. 2001;(2): 67–72.
  18. Затевалов АМ, Киселева ИА, Копанев ЮА, Алешкин АВ, Афанасьев СС, Селькова ЕП. Влияние бактериофагов на микрофлору толстой кишки. В: Материалы международной научно-практической конференции «Бактериофаги: Теоретические и практические аспекты применения в медицине, ветеринарии и пищевой промышленности», Ульяновск, 23–25 апреля 2013 г. Т. 2. Ульяновск: УГСХА им. П.А. Столыпина; 2013. с. 9–14.
  19. Verbeke KA, Boobis AR, Chiodini A, Edwards CA, Franck A, Kleerebezem M, Nauta A, Raes J, van Tol EA, Tuohy KM. Towards microbial fermentation metabolites as markers for health benefits of prebiotics. Nutr Res Rev. 2015;28(1): 42–66. doi: 10.1017/S0954422415000037.
  20. Mariat D, Firmesse O, Levenez F, Guimarăes V, Sokol H, Doré J, Corthier G, Furet JP. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 2009;9:123. doi: 10.1186/1471-2180-9-123.
  21. Agans R, Rigsbee L, Kenche H, Michail S, Khamis HJ, Paliy O. Distal gut microbiota of adolescent children is different from that of adults. FEMS Microbiol Ecol. 2011;77(2): 404– 12. doi: 10.1111/j.1574-6941.2011.01120.x.
  22. Balamurugan R, Janardhan HP, George S, Chittaranjan SP, Ramakrishna BS. Bacterial succession in the colon during childhood and adolescence: molecular studies in a southern Indian village. Am J Clin Nutr. 2008;88(6): 1643–7. doi: 10.3945/ajcn.2008.26511.
  23. Midtvedt AC, Carlstedt-Duke B, Midtvedt T. Establishment of a mucin-degrading intestinal microflora during the first two years of human life. J Pediatr Gastroenterol Nutr. 1994;18(3): 321–6.
  24. Derrien M, van Passel MW, van de Bovenkamp JH, Schipper RG, de Vos WM, Dekker J. Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes. 2010;1(4): 254–68. doi: 10.4161/gmic.1.4.12778.
  25. Lagkouvardos I, Kläring K, Heinzmann SS, Platz S, Scholz B, Engel KH, Schmitt-Kopplin P, Haller D, Rohn S, Skurk T, Clavel T. Gut metabolites and bacterial community networks during a pilot intervention study with flaxseeds in healthy adult men. Mol Nutr Food Res. 2015;59(8): 1614–28. doi: 10.1002/mnfr.201500125.
  26. Gill CI, Heavey P, McConville E, Bradbury I, Fässler C, Mueller S, Cresci A, Dore J, Norin E, Rowland I. Effect of fecal water on an in vitro model of colonic mucosal barrier function. Nutr Cancer. 2007;57(1): 59–65. doi: 10.1080/01635580701268220.

Supplementary files

There are no supplementary files to display.


Copyright (c) 2018 Zatevalov A.M., Selkova E.P., Gudova N.V., Oganesyan A.S.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies