Age-related changes in production of short chain fatty acids by oropharyngeal microbiota in patients without respiratory tract and oral disorders

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Abstract

Rationale: Functional activity of upper respiratory tract and oral microbiota has a high informational potential for diagnostics of infectious disease and for development of preventive measure, which is to be explained by rapid variability and high activity of bacteria in this location.

Aim: To determine statistical characteristics of concentrations and ratios of the oropharyngeal short chain fatty acids (SCFA) (i.e., functional activity of oropharyngeal microbiota) depending on age of patients without infectious disorder of upper respiratory tract and oral cavity.

Materials and methods: Gas liquid chromatography was used to measure SCFA concentrations in saliva from 683 patients aged from 1 month to 85 years who did not have any infections of respiratory tract and oral cavity. Age intervals with homogenous salivary SCFA levels were determined with constant trends in their means (medians) with one-month accuracy. The resulting parameters for the identified age intervals were compared with Mann-Whitney test at 95% significance level (p < 0.05).

Results: There were no significant differences between median total SCFA levels (8.04 [4.85; 14.22] mmol/G) and median acetic acid levels (6.27 [3.79; 11.21] mmol/G) in saliva from patients of all ages from 1 month to 85 years. For all other parameters, from 2 to 3 steps of changes were found that occurred at the age of 4 months and 14 years. After the age of 14, the concentrations of propionic and butyric acid significantly increased, whereas those of valeric and caproic acids, as well as of the branched chain SCFA decreased. Correspondingly, after the age of 14, the mean structural index increased from 0.25 to 0.27 U (p < 0.05). The isoacid index decreased with age in two steps: at the age of 4 months from 1.89 to 1.04 U (p < 0.05) and later at the age of 14 years to 0.74 U (p < 0.05).

Conclusion: Salivary SCFA levels become stable at the age of 14. The structural index and the isoacid index are most sensitive to the integral changes in the microbiota composition. Analysis of the results of studies on metabolic functioning of microflora should be based on mathematic modeling and multifactorial statistics in three age intervals: from birth to 4 months of age, from 4 months to 14 years and over 14 years.

About the authors

A. M. Zatevalov

G.N. Gabrichevsky Moscow Research Institute of Epidemiology and Microbiology

Author for correspondence.
Email: 89057149114@mail.ru

Alexander M. Zatevalov – PhD, ScD in Biology, Chief Research Fellow, Laboratory of Diagnosis and Prevention of Infectious Diseases

11–5 Detskaya ul., Zheleznodorozhny town, Moscow Region, 143985

Россия

E. P. Selkova

G.N. 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

Россия

N. V. Gudova

G.N. 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

Россия

A. S. Oganesyan

G.N. 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

Россия

References

  1. Алешкин ВА, Афанасьев СС, Караулова АВ, ред. Микробиоценозы и здоровье человека: руководство для врачей. М.: Династия; 2015. 548 с.
  2. Медведева ЕА, Мескина ЕР. Метаболическая активность микрофлоры ротоглотки у детей с бронхитом и внебольничной пневмонией. Альманах клинической медицины. 2015;42:72–8. doi: 10.18786/2072-0505-201542-72-78.
  3. Zaura E, Keijser BJ, Huse SM, Crielaard W. Defning the healthy "core microbiome" of oral microbial communities. BMC Microbiol. 2009;9:259. doi: 10.1186/1471-2180-9-259.
  4. Xian P, Xuedong Z, Xin X, Yuqing L, Yan L, Jiyao L, Xiaoquan S, Shi H, Jian X, Ga L. The oral microbiome bank of China. Int J Oral Sci. 2018;10(2):16. doi: 10.1038/s41368-0180018-x.
  5. Li K, Bihan M, Methé BA. Analyses of the stability and core taxonomic memberships of the human microbiome. PLoS One. 2013;8(5):e63139. doi: 10.1371/journal.pone.0063139.
  6. 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. Specifc 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.
  7. Bozzetto S, Pirillo P, Carraro S, Berardi M, Cesca L, Stocchero M, Giordano G, Zanconato S, Baraldi E. Metabolomic profle of children with recurrent respiratory infections. Pharmacol Res. 2017;115:162–7. doi: 10.1016/j.phrs.2016.11.007.
  8. Shirasugi M, Nishioka K, Yamamoto T, Nakaya T, Kanamura N. Normal human gingival fbroblasts undergo cytostasis and apoptosis after long-term exposure to butyric acid. Biochem Biophys Res Commun. 2017;482(4):1122–8. doi: 10.1016/j.bbrc.2016.11.168.
  9. Jenkinson HF. Beyond the oral microbiome. Environ Microbiol. 2011;13(12):3077–87. doi: 10.1111/j.1462-2920.2011.02573.x.
  10. Fan X, Alekseyenko AV, Wu J, Peters BA, Jacobs EJ, Gapstur SM, Purdue MP, Abnet CC, Stolzenberg-Solomon R, Miller G, Ravel J, Hayes RB, Ahn J. Human oral microbiome and prospective risk for pancreatic cancer: a population-based nested case-control study. Gut. 2018;67(1):120–7. doi: 10.1136/gutjnl-2016-312580.
  11. Jorth P, Turner KH, Gumus P, Nizam N, Buduneli N, Whiteley M. Metatranscriptomics of the human oral microbiome during health and disease. MBio. 2014;5(2):e01012–14. doi: 10.1128/mBio.01012-14.
  12. Lohavanichbutr P, Zhang Y, Wang P, Gu H, Nagana Gowda GA, Djukovic D, Buas MF, Raftery D, Chen C. Salivary metabolite profling distinguishes patients with oral cavity squamous cell carcinoma from normal controls. PLoS One. 2018;13(9):e0204249. doi: 10.1371/journal.pone.0204249.
  13. Ohshima M, Sugahara K, Kasahara K, Katakura A. Metabolomic analysis of the saliva of Japanese patients with oral squamous cell carcinoma. Oncol Rep. 2017;37(5):2727–34. doi: 10.3892/or.2017.5561.
  14. Huang CB, Alimova Y, Myers TM, Ebersole JL. Shortand medium-chain fatty acids exhibit antimicrobial activity for oral microorganisms. Arch Oral Biol. 2011;56(7):650–4. doi: 10.1016/j.archoralbio.2011.01.011.
  15. Алешкин ВА, Ардатская МД, Бабин ВН, Дубинин АВ, Иконников НС, Кондракова ОА, Минушкин ОН, авторы; НИФ «Ультрасан», заявитель и патентообладатель. Способ разделения смеси жирных кислот фракции С 2–С7 методом газожидкостной хроматографии. Пат. 2145511 Рос. Федерация. Опубл. 20.02.2000.
  16. Алешкин ВА, Селькова ЕП, Затевалов АМ, Миронов АЮ, Волчецкий АЛ, Гудова НВ. Определение дисбиотических изменений желудочно-кишечного тракта по маркерам содержимого кишечника. Федеральные клинические рекомендации. Нижний Новгород: Ремедиум Приволжье; 2016. 40 с.
  17. Алешкин ВА, Галимзянов ХМ, Афанасьев СС, Караулов АВ, Рубальский ОВ, Несвижский ЮВ, Воропаева ЕА, Афанасьев МС. Нарушения микробиоценозов у детей: Многоцентровое исследование. Cообщение I. Микробиоценоз и дисбактериоз ротоглотки у детей. Астраханский медицинский журнал. 2010;5(3):9–13.
  18. Анурова АЕ, Величко ЭВ, Косырева ТФ, Стуров НВ. Влияние микрофлоры полости рта матерей на формирование микробиоценоза полости рта у детей с врожденными расщелинами верхней губы и нёба. Трудный пациент. 2017;15(1–2):59–63.
  19. Затевалов АМ, Селькова ЕП, Гудова НВ, Оганесян АС. Возрастная динамика продукции короткоцепочечных жирных кислот кишечной микробиотой у пациентов, не имеющих гастроэнтерологических заболеваний. Альманах клинической медицины. 2018;46(2): 109–17. doi: 10.18786/2072-0505-2018-46-2109-117.
  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

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

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