Carbohydrate metabolism and the species composition of the intestinal microbiota in women with gestational diabetes mellitus

Cover Page


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

BACKGROUND: The prevalence of gestational diabetes mellitus has increased significantly and has become a global health problem, affecting 9.3–25.5% of pregnant women worldwide. Violation of the interaction of various body systems with the intestinal microbiota can be the cause of the development of insulin resistance. The study of the state of the intestinal microbiota based on the results of the study of the species composition of microorganisms in feces by the polymerase chain reaction method is necessary to understand the mechanisms of gestational diabetes mellitus development.

AIM: The aim of this study was to evaluate the intestinal microbiota status in women with normal pregnancy and pregnancy complicated by gestational diabetes mellitus.

MATERIALS AND METHODS: We examined 51 pregnant women in the period 2020-2022. The average age of women with normal pregnancy (n = 20) and pregnancy complicated by gestational diabetes mellitus (n = 31) was 29 (27.0; 32.5) and 31 (27.0; 35.0) years, respectively. The intestinal microbiota status was assessed based on the microbial species composition in feces using real-time polymerase chain reaction. All women underwent a test for carbohydrate metabolism at various gestation periods.

RESULTS: We have established a positive relation between Bacteroides thetaiotaomicron and Body Mass Index before pregnancy (r = 0.42). The number of Bacteroides thetaiotaomicron in the 1st, 2nd and 3rd trimesters of gestation positively correlated with the initial weight of women before pregnancy (r = 0.60, r = 0.52, r = 0.47, respectively; p < 0.05). The Bacteroides spp. / Faecalibacterium prausnitzii ratio in women with gestational diabetes mellitus was negatively correlated with the average blood glucose level in the 3rd trimester of pregnancy (r = –0.81; p < 0.05). Parvimonas micra positively correlated with venous plasma glucose levels in the presence of gestational diabetes mellitus (r = 0.58; p < 0.05). A positive relationship was obtained between the number of Escherichia coli in pregnant women in the 1st trimester and the average glucose level in the 3rd trimester of pregnancy (r = 0.41; p < 0.05). It was demonstrated that the growth of Bacteroides fragilis in the large intestine of pregnant women with gestational diabetes mellitus in the 3rd trimester of pregnancy correlated with subnormal blood glucose levels (r = –0.77; p < 0.05), which may be due to a diet disorder (insufficient carbohydrate intake) or insulin overdose, which can lead to hypoglycemic conditions. In the group of women with gestational diabetes mellitus, a positive correlation was obtained between glycated hemoglobin level and the opportunistic pathogen Klebsiella pneumoniae representative amount in the 1st trimester of pregnancy (r = 0.46; p < 0.05). In addition, we have found positive relations between the Citrobacter spp. / Enterobacter spp. ratio and the maximum blood glucose level in women with gestational diabetes mellitus in the 1st, 2nd and 3rd trimesters of pregnancy (r = 0.49, r = 0.43, r = 0.47, respectively; p < 0.05). The difference in the intake of dietary fiber in the control group and in the group of pregnant women with gestational diabetes mellitus was obtained: 2 (1; 3) and 1 (1; 1), respectively (p < 0.05).

CONCLUSIONS: Data have been obtained confirming the relationship between disorders of the colon microbiocenosis and carbohydrate metabolism in pregnant women with gestational diabetes mellitus. A relationship has been found between insufficient intake of dietary fiber and the risk of developing gestational diabetes mellitus.

Full Text

Restricted Access

About the authors

Tatyana A. Zinina

Women’s Consultation No. 22

Email: zininat@mail.ru

MD

Russian Federation, Saint Petersburg

Alena V. Tiselko

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

Author for correspondence.
Email: alenadoc@mail.ru
ORCID iD: 0000-0002-2512-833X
SPIN-code: 5644-9891
Scopus Author ID: 57194216306

MD, Dr. Sci. (Med.)

Russian Federation, Saint Petersburg

Maria I. Yarmolinskaya

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

Email: m.yarmolinskaya@gmail.com
ORCID iD: 0000-0002-6551-4147
SPIN-code: 3686-3605
Scopus Author ID: 7801562649
ResearcherId: P-2183-2014

MD, Dr. Sci. (Med.), Professor, Professor of the Russian Academy of Sciences

Russian Federation, Saint Petersburg

References

  1. Zhong H, Zhang J, Xia J, et al. Influence of gestational diabetes mellitus on lipid signatures in breast milk and association with fetal physical development. Front Nutr. 2022;9. doi: 10.3389/fnut.2022.924301
  2. Yang T, Santisteban MM, Rodriguez V, et al. Gut dysbiosis is linked to hypertension. Hypertension. 2015;65(6):1331–1340. doi: 10.1161/HYPERTENSIONAHA.115.05315
  3. Cortez RV, Taddei CR, Sparvoli LG, et al. Microbiome and its relation to gestational diabetes. Endocrine. 2019;64(2):254–264. doi: 10.1007/s12020-018-1813-z
  4. Nirmalkar K, Murugesan S, Pizano-Zárate ML, et al. Gut microbiota and endothelial dysfunction markers in obese mexican children and adolescents. Nutrients. 2018;10(12). doi: 10.3390/nu10122009
  5. Wang B, Yao M, Lv L, et al. The human microbiota in health and disease. Engineering. 2017;3(1):71–82. doi: 10.1016/J.ENG.2017.01.008
  6. Shestakova EA, Pokrovskaya EV, Samsonova MD. Different approaches to change gut microbiota and its influence on metabolic disorders. Consilium Medicum. 2021;23(12):905–909. (In Russ.) doi: 10.26442/20751753.2021.12.201289
  7. Kravchuk EN, Neimark AE, Grineva EN, et al. The role of gut microbiota in metabolic regulation. Diabetes Mellitus. 2016;19(4):280–285. (In Russ.) doi: 10.14341/DM7704
  8. Guinane CM, Cotter PD. Role of the gut microbiota in health and chronic gastrointestinal disease: understanding a hidden metabolic organ. Therap Adv Gastroenterol. 2013;6(4):295–308. doi: 10.1177/1756283X13482996
  9. Rinninella E, Raoul P, Cintoni M, et al. What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases. Microorganisms. 2019;7(1). doi: 10.3390/microorganisms7010014
  10. Gasmi A, Mujawdiya PK, Pivina L, et al. Relationship between gut microbiota, gut hyperpermeability and obesity. Curr Med Chem. 2021;28(4):827–839. doi: 10.2174/0929867327666200721160313
  11. Thursby E, Juge N. Introduction to the human gut microbiota. Biochem J. 2017;474(11):1823–1836. doi: 10.1042/BCJ20160510
  12. Gilbert JA, Blaser MJ, Caporaso JG, et al. Current under standing of the human microbiome. Nat Med. 2018;24(4):392–400. doi: 10.1038/nm.4517
  13. Koren O, Goodrich JK, Cullender TC, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012;150(3):470–480. doi: 10.1016/j.cell.2012.07.008
  14. Medici Dualib P, Ogassavara J, Mattar R, et al. Gut microbiota and gestational diabetes mellitus: a systematic review. Diabetes Res Clin Pract. 2021;180. doi: 10.1016/j.diabres.2021.109078
  15. Ibragimova LI, Kolpakova EA, Dzagakhova AV, et al. The role of the gut microbiota in the development of type 1 diabetes mellitus. Diabetes mellitus. 2021;24(1):62–69. (In Russ.) doi: 10.14341/DM10326
  16. Dzgoeva FH, Egshatyan LV. The gut microbiota and type 2 diabetes mellitus. Endocrinologiya: novosti, mneniya, obuchenie. 2018;3(24):55–63. (In Russ.) doi: 10.24411/2304-9529-2018-13005
  17. Huang L, Thonusin C, Chattipakorn N, et al. Impacts of gut microbiota on gestational diabetes mellitus: a comprehensive review. Eur J Nutr. 2021;60(5):2343–2360. doi: 10.1007/s00394-021-02483-6
  18. Vetrani C, Di Nisio A, Paschou SA, et al. From gut microbiota through low-grade inflammation to obesity: key players and potential targets. Nutrients. 2022;14(10). doi: 10.3390/nu14102103
  19. Youm YH, Nguyen KY, Grant RW, et al. The ketone metabolite β-hydroxybutyrate blocks NLRP3 inflammasome-mediated inflammatory disease. Nat Med. 2015;21(3):263–269. doi: 10.1038/nm.3804
  20. Macia L, Tan J, Vieira A, et al. Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome. Nat Commun. 2015;6. doi: 10.1038/ncomms7734
  21. Saltzman ET, Palacios T, Thomsen M, et al. Intestinal microbiome shifts, dysbiosis, inflammation, and non-alcoholic fatty liver disease. Front Microbiol. 2018;9. doi: 10.3389/fmicb.2018.00061
  22. Zhu LB, Zhang YC, Huang HH, et al. Prospects for clinical applications of butyrate-producing bacteria. World J Clin Pediatr. 2021;10(5):84–92. doi: 10.5409/wjcp.v10.i5.84
  23. Sugawara T, Iwamoto N, Akashi M, et al. Tight junction dysfunction in the stratum granulosum leads to aberrant stratum corneum barrier function in claudin-1-deficient mice. J Dermatol Sci. 2013;70(1):12–18. doi: 10.1016/j.jdermsci.2013.01.002
  24. Mokkala K, Röytiö H, Munukka E, et al. Gut microbiota richness and composition and dietary intake of overweight pregnant women are related to serum zonulin concentration, a marker for intestinal permeability. J Nutr. 2016;146(9):1694–1700. doi: 10.3945/jn.116.235358
  25. Egshatyan L, Kashtanova D, Popenko A, et al. Gut microbiota and diet in patients with different glucose tolerance. Endocr Connect. 2016;5(1):1–9. doi: 10.1530/EC-15-0094
  26. Sharon I, Quijada NM, Pasolli E, et al. The core human microbiome: does it exist and how can we find it? A critical review of the concept. Nutrients. 2022;14(14). doi: 10.3390/nu14142872
  27. Qasim A, Turcotte M, de Souza RJ, et al. On the origin of obesity: identifying the biological, environmental and cultural drivers of genetic risk among human populations. Obes Rev. 2018;19(2):121–149. doi: 10.1111/obr.12625
  28. Rossiiskaya assotsiatsiya endokrinologov, Rossiiskoe obshchest vo akusherov-ginekologov. Gestatsionnyi sakharnyi diabet. Diagnostika, lechenie, akusherskaya taktika, poslerodovoe nablyudenie: klinicheskie rekomendatsii. 2020. (In Russ.) [cited 2022 Jul 15]. Availaible from: https://rae-org.ru/system/files/documents/pdf/kr_gsd_2020.pdf
  29. Neuman H, Koren O. The pregnancy microbiome. Nestle Nutr Inst Workshop Ser. 2017;88:1–9. doi: 10.1159/000455207
  30. Nuriel-Ohayon M, Neuman H, Ziv O, et al. Progesterone increases bifidobacterium relative abundance during late pregnancy. Cell Rep. 2019;27(3):730–736. doi: 10.1016/j.celrep.2019.03.075
  31. Ferrarese R, Ceresola ER, Preti A, et al. Probiotics, prebiotics and synbiotics for weight loss and metabolic syndrome in the microbiome era. Eur Rev Med Pharmacol Sci. 2018;22(21):7588–7605. doi: 10.26355/eurrev_201811_16301
  32. Farhat S, Hemmatabadi M, Ejtahed HS, et al. Microbiome alterations in women with gestational diabetes mellitus and their offspring: a systematic review. Front Endocrinol (Lausanne). 2022;13. doi: 10.3389/fendo.2022.1060488
  33. Zhang X, Wang P, Ma L, et al. Differences in the oral and intestinal microbiotas in pregnant women varying in periodontitis and gestational diabetes mellitus conditions. J Oral Microbiol. 2021;13(1). doi: 10.1080/20002297.2021.1883382
  34. Cui MJ, Qi C, Yang LP, et al. A pregnancy complication-dependent change in SIgA-targeted microbiota during third trimester. Food Funct. 2020;11(2):1513–1524. doi: 10.1039/C9FO02919B
  35. Sitkin SI, Vahitov TY, Demyanova EV. Microbiome, colon dysbiosis and inflammatory bowel disease: when function affects taxo nomy. Almanac of clinical medicine. 2018;46(5):396–425. (In Russ.) doi: 10.18786/2072-0505-2018-46-5-396-425
  36. Wei J, Qing Y, Zhou H, et al. 16S rRNA gene amplicon sequencing of gut microbiota in gestational diabetes mellitus and their correlation with disease risk factors. J Endocrinol Invest. 2022;45(2):279–289. doi: 10.1007/s40618-021-01595-4
  37. Sililas P, Huang L, Thonusin C, et al. Association between gut microbiota and development of gestational diabetes mellitus. Microorganisms. 2021;9(8). doi: 10.3390/microorganisms9081686
  38. Mokkala K, Paulin N, Houttu N, et al. Metagenomics analysis of gut microbiota in response to diet intervention and gestational diabetes in overweight and obese women: a randomised, double-blind, placebo-controlled clinical trial. Gut. 2021;70(2):309–318. doi: 10.1136/gutjnl-2020-321643
  39. Hou M, Li F. Changes of intestinal flora, cellular immune function and inflammatory factors in Chinese advanced maternal age with gestational diabetes mellitus. Acta Med Mediterr. 2020;36(2):1137–1142. doi: 10.19193/0393-6384_2020_2_178
  40. Chen T, Zhang Y, Zhang Y, et al. Relationships between gut microbiota, plasma glucose and gestational diabetes mellitus. J Diabetes Investig. 2021;12(4):641–650. doi: 10.1111/jdi.13373
  41. Wen H, Gris D, Lei Y, et al. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol. 2011;12(5):408–415. doi: 10.1038/ni.2022
  42. Progatzky F, Sangha NJ, Yoshida N, et al. Dietary cholesterol directly induces acute inflammasome-dependent intestinal inflammation. Nat Commun. 2014;5. doi: 10.1038/ncomms6864
  43. Volkova NI, Naboka YL, Ganenko LA, et al. A feature of the microbiota of the colon in patients with different phenotypes of obesity (pilot study). Medical Herald of the South of Russia. 2020;11(2):38–45. (In Russ.) doi: 10.21886/2219-8075-2020-11-2-38-45

Supplementary files

Supplementary Files
Action
1. JATS XML
2. Fig. 1. Correlations of intestinal microbiocenosis with carbohydrate metabolism parameters in the group of women with gestational diabetes mellitus. Mean, average glucose level; Max, the highest level of glucose; тр., trimester; ОВ, total bacterial count; LBGI, low blood glucose Index; HbA1c, glycated hemoglobin; GDM, gestational diabetes mellitus; BMI, body mass index. * p < 0.05

Download (327KB)
3. Fig. 2. Opportunistic flora (a) and normobiocenosis (b) distribution in women with normal pregnancy (Сontrol) and pregnancy complicated by gestational diabetes mellitus (GDM) (0 % of the species representatives means no excess of colony-forming units per 1 g of content in the distal colon intestines, accepted as the norm)

Download (362KB)

Copyright (c) 2023 Eсо-Vector



СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 66759 от 08.08.2016 г. 
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия Эл № 77 - 6389
от 15.07.2002 г.



This website uses cookies

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

About Cookies