Gut Microbiota Shift in Obese Adolescents Born by Cesarean Section

Evgenia A. Novikova, Natalia L. Belkova, Anna V. Pogodina, Anastasia I. Romanitsa, Elizaveta S. Klimenko, Uliana M. Nemchenko, Lyubov V. Rychkova

 
International Journal of Biomedicine. 2020;10(4):424-429.
DOI: 10.21103/Article10(4)_OA19
Originally published December 10, 2020

Abstract: 

Background: It is known that in the early postnatal period a variety of factors affect the gut microbiota (GM) composition, including delivery mode. The effect of delivery mode on the human GM in the late postnatal period remains unexplored. A shift of GM composition due to delivery mode may contribute to the development of obesity in adulthood.
Methods and Results: The study included six adolescents aged between 11 and 17 years treated and examined at the Clinic of the Scientific Center for Family Health and Human Reproduction (Irkutsk, Russia) in 2016. Stool samples were collected following the standard operating procedures according to the International Human Microbiome Standards. Metasequencing of V3-V4 variable regions of the 16S rRNA gene was performed by the Novogene Company (China) on the Illumina platform. Bioinformatic analysis was done by the bri-shur.com services. Sequencing reads were presented as normalized values.
In general, the GM composition of obese adolescents born by cesarean section was characterized by composition heterogeneity within the Bacteroidetes phylum and the dominance of certain phylotypes as signs of dysbiosis for each adolescent. We detected an increased abundance of phyla Bacteroides and Proteobacteria, and an absence of Tenericutes in obese adolescents born by Caesarean section. On the level of genera, the prevalence of Bacteroides and Bacteroides S24-7 phylotypes, and the absence of the RF39 phylotype, led to the GM shift associated with a cesarean section or obesity.
Conclusion: Obese adolescents born by cesarean section delivery present the shift in GM composition.

Keywords: 
gut microbiota • dysbiosis • amplicon metasequencing • cesarean section • vaginal birth • obesity • adolescents
References: 

1. Kim G, Bae J, Kim MJ, Kwon H, Park G, Kim S-J et al. Delayed Establishment of Gut Microbiota in Infants Delivered by Cesarean Section. Front Microbiol. 2020 Sep 11;11:2099. doi: 10.3389/fmicb.2020.02099.
2. Madan JC, Hoen AG, Lundgren SN, Farzan SF, Cottingham KL, Morrison HG, et al. Association of Cesarean Delivery and Formula Supplementation With the Intestinal Microbiome of 6-Week-Old Infants. JAMA Pediatr. 2016;170(3):212-9. doi: 10.1001/jamapediatrics.2015.3732.
3. Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS, et al.; CHILD Study Investigators. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ. 2013;185(5):385-94. doi: 10.1503/cmaj.121189.
4. Reyman M, van Houten MA, van Baarle D, Bosch AATM, Man WH, Chu MLJN, wt al. Impact of delivery mode-associated gut microbiota dynamics on health in the first year of life. Nat Commun. 2019 Nov 1;10(1):4997. doi: 10.1038/s41467-019-13014-7. Erratum in: Nat Commun. 2019 Nov 25;10(1):5352. 
5. Belkova NL, Nemchenko UM, Pogodina AV, Feranchuk SI, Romanitsa AI, Novikova EA, Rychkova LV. Composition and Structure of Gut Microbiome in Adolescents with Obesity and Different Breastfeeding Duration. Bull Exp Biol Med. 2019 Oct;167(6):759-762. doi: 10.1007/s10517-019-04617-7. 
6. Pannaraj PS, Li F, Cerini C, Bender JM, Yang S, Rollie A, Adisetiyo H, Zabih S, Lincez PJ, Bittinger K, Bailey A, Bushman FD, Sleasman JW, Aldrovandi GM. Association Between Breast Milk Bacterial Communities and Establishment and Development of the Infant Gut Microbiome. JAMA Pediatr. 2017 Jul 1;171(7):647-654. doi: 10.1001/jamapediatrics.2017.0378. 
7. Fjalstad JW, Esaiassen E, Juvet LK, van den Anker JN, Klingenberg C. Antibiotic therapy in neonates and impact on gut microbiota and antibiotic resistance development: a systematic review. J Antimicrob Chemother. 2018 Mar 1;73(3):569-580. doi: 10.1093/jac/dkx426. 
8. Gosalbes MJ, Llop S, Vallès Y, Moya A, Ballester F, Francino MP. Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clin Exp Allergy. 2013 Feb;43(2):198-211. doi: 10.1111/cea.12063.
9. Wang L, Gong Z, Huo J, Zhuo Q, Qin W, Yang Z, Wang J, Shen S. [Effects of nutrition package on intestinal flora of infants by high-throughput sequencing]. Wei Sheng Yan Jiu. 2020 Mar;49(2):233-237. Chinese. doi: 10.19813/j.cnki.weishengyanjiu.2020.02.011. [Article in Chinese].
10. Mueller NT, Bakacs E, Combellick J, Grigoryan Z, Dominguez-Bello MG. The infant microbiome development: mom matters. Trends Mol Med. 2015 Feb;21(2):109-17. doi: 10.1016/j.molmed.2014.12.002. E
11. Marques TM, Wall R, Ross RP, Fitzgerald GF, Ryan CA, Stanton C. Programming infant gut microbiota: influence of dietary and environmental factors. Curr Opin Biotechnol. 2010 Apr;21(2):149-56. doi: 10.1016/j.copbio.2010.03.020. 
12. Nikolaeva IV, Tsaregorodtsev AD, Shaikhieva GS. [Formation of the intestinal microbiota of children and the factors that influence this process]. Rossiyskiy Vestnik Perinatologii i Pediatrii (Russian Bulletin of Perinatology and Pediatrics). 2018;63(3):13-8. doi: 10.21508/1027-4065-2018-63-3-13-18.p [Article in Russian].
13. Huurre A, Kalliomäki M, Rautava S, Rinne M, Salminen S, Isolauri E. Mode of delivery - effects on gut microbiota and humoral immunity. Neonatology. 2008;93(4):236-40. doi: 10.1159/000111102. 
14. Miettinen R, Hermansson H, Merikukka M, Gissler M, Isolauri E. Mode of delivery--impact on risk of noncommunicable diseases. J Allergy Clin Immunol. 2015 Nov;136(5):1398-9. doi: 10.1016/j.jaci.2015.05.032.
15. Kalliomäki M, Collado MC, Salminen S, Isolauri E. Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr. 2008 Mar;87(3):534-8. doi: 10.1093/ajcn/87.3.534. 
16. WHO. Obesity and overweight. Available at: https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight (accessed 2020 September 30).
17. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972 Jun;18(6):499-502. 
18. Styne DM, Arslanian SA, Connor EL, Farooqi IS, Murad MH, Silverstein JH, Yanovski JA. Pediatric Obesity-Assessment, Treatment, and Prevention: An Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab. 2017 Mar 1;102(3):709-757. doi: 10.1210/jc.2016-2573. 
19. Klimov AN. Causes and conditions of atherosclerosis development. In: Kositsky GI, editors. Preventive cardiology. Moscow: Meditsina; 1977:260-321.[In Russian].
20. Feranchuk S, Belkova N, Potapova U, Ochirov I, Kuzmin D, Belikov S. [Tools and a web server for data analysis and visualization in microbial ecology]. Community Ecology. 2019;20(2):230-237.[Article in Russian]
21. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006 Dec 21;444(7122):1022-3. doi: 10.1038/4441022a.
22. Tenaillon O, Skurnik D, Picard B, Denamur E. The population genetics of commensal Escherichia coli. Nat Rev Microbiol. 2010 Mar;8(3):207-17. doi: 10.1038/nrmicro2298.
23. Brubaker RR. Physiology of Yersinia pestis. Adv Exp Med Biol. 2016;918:79-99. doi: 10.1007/978-94-024-0890-4_4. 
24. Hidalgo-Cantabrana C, Delgado S, Ruiz L, Ruas-Madiedo P, Sánchez B, Margolles A. Bifidobacteria and Their Health-Promoting Effects. Microbiol Spectr. 2017 Jun;5(3). doi: 10.1128/microbiolspec.BAD-0010-2016. 
25. Geerlings SY, Kostopoulos I, de Vos WM, Belzer C. Akkermansia muciniphila in the Human Gastrointestinal Tract: When, Where, and How? Microorganisms. 2018 Jul 23;6(3):75. doi: 10.3390/microorganisms6030075. 
26. Trachtenberg S. Mollicutes. Curr Biol. 2005 Jul 12;15(13):R483-4. doi: 10.1016/j.cub.2005.06.049. 
27. Magnúsdóttir S, Thiele I. Modeling metabolism of the human gut microbiome. Curr Opin Biotechnol. 2018 Jun;51:90-96. doi: 10.1016/j.copbio.2017.12.005.

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Received October 2, 2020.
Accepted November 8, 2020.
©2020 International Medical Research and Development Corporation.