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Research Paper

Parity modulates impact of BMI and gestational weight gain on gut microbiota in human pregnancy

ORCID Icon, , , , , , , , & ORCID Icon show all
Article: 2259316 | Received 29 Jun 2023, Accepted 12 Sep 2023, Published online: 09 Oct 2023

References

  • Tan EK, Tan EL. Alterations in physiology and anatomy during pregnancy. Best Pract Res Clin Obstet Gynaecol. 2013;27(6):791–21. doi:10.1016/j.bpobgyn.2013.08.001.
  • Poston L, Caleyachetty R, Cnattingius S, Corvalán C, Uauy R, Herring S, Gillman MW. Preconceptional and maternal obesity: epidemiology and health consequences. Lancet Diabetes Endocrinol. 2016;4(12):1025–1036. doi:10.1016/S2213-8587(16)30217-0.
  • Yeo E, Brubaker PL, Sloboda DM. The intestine and the microbiota in maternal glucose homeostasis during pregnancy. J Endocrinol. 2022;253(1):R1–R19. doi:10.1530/JOE-21-0354.
  • Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Bäckhed HK, Gonzalez A, Werner J, Angenent L, Knight R, 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.
  • Faucher MA, Greathouse KL, Hastings-Tolsma M, Padgett RN, Sakovich K, Choudhury A, Sheikh A, Ajami NJ, Petrosino JF. Exploration of the vaginal and gut microbiome in African American women by body mass index, class of obesity, and gestational weight gain: a pilot study. Am J Perinatol. 2020;37(11):1160–1172. doi:10.1055/s-0039-1692715.
  • DiGiulio DB, Callahan BJ, McMurdie PJ, Costello EK, Lyell DJ, Robaczewska A, Sun CL, Goltsman DSA, Wong RJ, Shaw G, et al. Temporal and spatial variation of the human microbiota during pregnancy. Proc Natl Acad Sci U S A. 2015;112(35):11060–11065. doi:10.1073/pnas.1502875112.
  • Kumbhare SV, Patangia DV, Mongad DS, Bora A, Bavdekar AR, Shouche YS. Gut microbial diversity during pregnancy and early infancy: an exploratory study in the Indian population. FEMS Microbiol Lett. 2020;367(3):367. doi:10.1093/femsle/fnaa022.
  • Qin S, Liu Y, Wang S, Ma J, Yang H. Distribution characteristics of intestinal microbiota during pregnancy and postpartum in healthy women. J Matern Fetal Neonatal Med. 2021;1–8. doi:10.1080/14767058.2020.1812571.
  • Goltsman DSA, Sun CL, Proctor DM, DiGiulio DB, Robaczewska A, Thomas BC, Shaw GM, Stevenson DK, Holmes SP, Banfield JF, et al. Metagenomic analysis with strain-level resolution reveals fine-scale variation in the human pregnancy microbiome. Genome Res. 2018;28(10):1467–1480. doi:10.1101/gr.236000.118.
  • Yang H, Guo R, Li S, Liang F, Tian C, Zhao X, Long Y, Liu F, Jiang M, Zhang Y, et al. Systematic analysis of gut microbiota in pregnant women and its correlations with individual heterogeneity. NPJ Biofilms Microbiomes. 2020;6(1):32. doi:10.1038/s41522-020-00142-y.
  • Gohir W, Ratcliffe EM, Sloboda DM. Of the bugs that shape us: maternal obesity, the gut microbiome, and long-term disease risk. Pediatr Res. 2015;77(1–2):196–204. doi:10.1038/pr.2014.169.
  • Gluckman PD, Hanson MA. Maternal constraint of fetal growth and its consequences. Semin Fetal Neonatal Med. 2004;9(5):419–425. doi:10.1016/j.siny.2004.03.001.
  • Kennedy KM, Gerlach MJ, Adam T, Heimesaat MM, Rossi L, Surette MG, Sloboda DM, Braun T. Fetal meconium does not have a detectable microbiota before birth. Nature Microbiol. 2021;6(7):865–873. doi:10.1038/s41564-021-00904-0.
  • Kennedy KM, de Goffau MC, Perez-Muñoz ME, Arrieta MC, Bäckhed F, Bork P, Braun T, Bushman FD, Dore J, de Vos WM, et al. Questioning the fetal microbiome illustrates pitfalls of low-biomass microbial studies. Nature. 2023;613(7945):639–649. doi:10.1038/s41586-022-05546-8.
  • Deputy NP, Sharma AJ, Kim SY, Hinkle SN. Prevalence and characteristics associated with gestational weight gain adequacy. Obstet Gynecol. 2015;125(4):773–781. doi:10.1097/AOG.0000000000000739.
  • Rasmussen KM, Yaktine AL, editors. Weight gain during pregnancy: reexamining the guidelines. Washington (DC): National Academies Press (US); 2010. doi:10.17226/12584.
  • Santacruz A, Collado MC, García-Valdés L, Segura MT, Martín-Lagos JA, Anjos T, Martí-Romero M, Lopez RM, Florido J, Campoy C, et al. Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr. 2010;104(1):83–92. doi:10.1017/S0007114510000176.
  • Collado MC, Isolauri E, Laitinen K, Salminen S. Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am J Clin Nutr. 2008;88(4):894–899. doi:10.1093/ajcn/88.4.894.
  • Stanislawski MA, Dabelea D, Wagner BD, Sontag MK, Lozupone CA, Eggesbø M. Pre-pregnancy weight, gestational weight gain, and the gut microbiota of mothers and their infants. Microbiome. 2017;5(1):113. doi:10.1186/s40168-017-0332-0.
  • Aatsinki AK, Uusitupa HM, Munukka E, Pesonen H, Rintala A, Pietilä S, Lahti L, Eerola E, Karlsson L, Karlsson H, et al. Gut microbiota composition in mid-pregnancy is associated with gestational weight gain but not prepregnancy body mass index. J Womens Health. 2018;27(10):1293–1301. doi:10.1089/jwh.2017.6488.
  • Zacarías MF, Collado MC, Gómez-Gallego C, Flinck H, Aittoniemi J, Isolauri E, Salminen S. Pregestational overweight and obesity are associated with differences in gut microbiota composition and systemic inflammation in the third trimester. PloS One. 2018;13(7):e0200305. doi:10.1371/journal.pone.0200305.
  • Crusell MKW, Hansen TH, Nielsen T, Allin KH, Rühlemann MC, Damm P, Vestergaard H, Rørbye C, Jørgensen NR, Christiansen OB, et al. Gestational diabetes is associated with change in the gut microbiota composition in third trimester of pregnancy and postpartum. Microbiome. 2018;6(1):89. doi:10.1186/s40168-018-0472-x.
  • Abu-Heija AT, Al-Bash MR, Al-Kalbani MA. Effects of maternal age, parity and pre-pregnancy body mass index on the glucose challenge test and gestational diabetes mellitus. J Taibah Univ Med Sci. 2017;12(4):338–342. doi:10.1016/j.jtumed.2017.01.005.
  • Rifas-Shiman SL, Willett WC, Lobb R, Kotch J, Dart C, Gillman MW. PrimeScreen, a brief dietary screening tool: reproducibility and comparability with both a longer food frequency questionnaire and biomarkers. Public Health Nutr. 2001;4(2):249–254. doi:10.1079/phn200061.
  • Olsson LM, Boulund F, Nilsson S, Khan MT, Gummesson A, Fagerberg L, Engstrand L, Perkins R, Uhlén M, Bergström G, et al. Dynamics of the normal gut microbiota: a longitudinal one-year population study in Sweden. Cell Host & Microbe. 2022;30(5):726–739.e3. doi:10.1016/j.chom.2022.03.002.
  • Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. 2016;165(6):1332–1345. doi:10.1016/j.cell.2016.05.041.
  • Ezzine C, Loison L, Montbrion N, Bôle-Feysot C, Déchelotte P, Coëffier M, Ribet D. Fatty acids produced by the gut microbiota dampen host inflammatory responses by modulating intestinal SUMOylation. Gut Microbes. 2022;14(1):2108280. doi:10.1080/19490976.2022.2108280.
  • Heimann E, Nyman M, Pålbrink AK, Lindkvist-Petersson K, Degerman E. Branched short-chain fatty acids modulate glucose and lipid metabolism in primary adipocytes. Adipocyte. 2016;5(4):359–368. doi:10.1080/21623945.2016.1252011.
  • Wang B, Kong Q, Li X, Zhao J, Zhang H, Chen W, Wang G. A high-fat diet increases gut microbiota biodiversity and energy expenditure due to nutrient difference. Nutrients. 2020;12(10):12. doi:10.3390/nu12103197.
  • Ma L, Ni Y, Wang Z, Tu W, Ni L, Zhuge F, Zheng A, Hu L, Zhao Y, Zheng L, et al. Spermidine improves gut barrier integrity and gut microbiota function in diet-induced obese mice. Gut Microbes. 2020;12(1):1–19. doi:10.1080/19490976.2020.1832857.
  • Ma S, You Y, Huang L, Long S, Zhang J, Guo C, Zhang N, Wu X, Xiao Y, Tan H, et al. Alterations in gut microbiota of gestational diabetes patients during the first trimester of pregnancy. Front Cell Infect Microbiol. 2020;10:58. doi:10.3389/fcimb.2020.00058.
  • Fu J, Bonder MJ, Cenit MC, Tigchelaar EF, Maatman A, Dekens JAM, Brandsma E, Marczynska J, Imhann F, Weersma RK, et al. The gut microbiome contributes to a substantial proportion of the variation in blood lipids. Circ Res. 2015;117(9):817–824. doi:10.1161/CIRCRESAHA.115.306807.
  • Mueller NT, Bakacs E, Combellick J, Grigoryan Z, Dominguez-Bello MG. The infant microbiome development: mom matters. Trends Mol Med. 2015;21(2):109–117. doi:10.1016/j.molmed.2014.12.002.
  • Imoto N, Kano C, Aoyagi Y, Morita H, Amanuma F, Maruyama H, Nojiri S, Hashiguchi N, Watanabe S. Administration of β-lactam antibiotics and delivery method correlate with intestinal abundances of bifidobacteria and bacteroides in early infancy, in Japan. Sci Rep. 2021;11(1):6231. doi:10.1038/s41598-021-85670-z.
  • Mueller NT, Shin H, Pizoni A, Werlang IC, Matte U, Goldani MZ, Goldani HAS, Dominguez-Bello MG. Birth mode-dependent association between pre-pregnancy maternal weight status and the neonatal intestinal microbiome. Sci Rep. 2016;6(1):23133. doi:10.1038/srep23133.
  • Tun HM, Bridgman SL, Chari R, Field CJ, Guttman DS, Becker AB, Mandhane PJ, Turvey SE, Subbarao P, Sears MR, et al. Roles of birth mode and infant gut microbiota in intergenerational transmission of overweight and obesity from mother to offspring. JAMA Pediatr. 2018;172(4):368–377. doi:10.1001/jamapediatrics.2017.5535.
  • Collado MC, Isolauri E, Laitinen K, Salminen S. Effect of mother’s weight on infant’s microbiota acquisition, composition, and activity during early infancy: a prospective follow-up study initiated in early pregnancy. Am J Clin Nutr. 2010;92(5):1023–1030. doi:10.3945/ajcn.2010.29877.
  • Galley JD, Bailey M, Kamp Dush C, Schoppe-Sullivan S, Christian LM, Shankar K. Maternal obesity is associated with alterations in the gut microbiome in toddlers. PloS One. 2014;9(11):e113026. doi:10.1371/journal.pone.0113026.
  • Baumann-Dudenhoeffer AM, D’Souza AW, Tarr PI, Warner BB, Dantas G. Infant diet and maternal gestational weight gain predict early metabolic maturation of gut microbiomes. Nat Med. 2018;24(12):1822–1829. doi:10.1038/s41591-018-0216-2.
  • Robinson A, Fiechtner L, Roche B, Ajami NJ, Petrosino JF, Camargo CA, Taveras EM, Hasegawa K. Association of maternal gestational weight gain with the infant fecal microbiota. J Pediatr Gastroenterol Nutr. 2017;65(5):509–515. doi:10.1097/MPG.0000000000001566.
  • Benítez-Páez A, Gómez Del Pugar EM, López-Almela I, Moya-Pérez Á, Codoñer-Franch P, Sanz Y, Turnbaugh PJ. Depletion of Blautia species in the microbiota of obese children relates to intestinal inflammation and metabolic phenotype worsening. mSystems. 2020;5(2):5. doi:10.1128/mSystems.00857-19.
  • Singer K, Lumeng CN. The initiation of metabolic inflammation in childhood obesity. J Clin Invest. 2017;127(1):65–73. doi:10.1172/JCI88882.
  • Ferretti P, Pasolli E, Tett A, Asnicar F, Gorfer V, Fedi S, Armanini F, Truong DT, Manara S, Zolfo M, et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host & Microbe. 2018;24(1):133–145.e5. doi:10.1016/j.chom.2018.06.005.
  • Ruebel ML, Gilley SP, Sims CR, Zhong Y, Turner D, Chintapalli SV, Piccolo BD, Andres A, Shankar K. Associations between maternal diet, body composition and gut microbial ecology in pregnancy. Nutrients. 2021;13(9):3295. doi:10.3390/nu13093295.
  • Letourneau J, Holmes ZC, Dallow EP, Durand HK, Jiang S, Carrion VM, Gupta SK, Mincey AC, Muehlbauer MJ, Bain JR, et al. Ecological memory of prior nutrient exposure in the human gut microbiome. ISME J. 2022;16(11):2479–2490. doi:10.1038/s41396-022-01292-x.
  • Gomez-Arango LF, Barrett HL, McIntyre HD, Callaway LK, Morrison M, Dekker Nitert M. Connections between the gut microbiome and metabolic hormones in early pregnancy in overweight and obese women. Diabetes. 2016;65(8):2214–2223. doi:10.2337/db16-0278.
  • Fassarella M, Blaak EE, Penders J, Nauta A, Smidt H, Zoetendal EG. Gut microbiome stability and resilience: elucidating the response to perturbations in order to modulate gut health. Gut. 2021;70(3):595–605. doi:10.1136/gutjnl-2020-321747.
  • Mouzon SH, Lassance L. Endocrine and metabolic adaptations to pregnancy; impact of obesity. Horm Mol Biol Clin Investig. 2015;24(1):65–72. doi:10.1515/hmbci-2015-0042.
  • Forbes S, Barr SM, Reynolds RM, Semple S, Gray C, Andrew R, Denison FC, Walker BR, Norman JE. Convergence in insulin resistance between very severely obese and lean women at the end of pregnancy. Diabetologia. 2015;58(11):2615–2626. doi:10.1007/s00125-015-3708-3.
  • Tinius RA, Blankenship MM, Furgal KE, Cade WT, Pearson KJ, Rowland NS, Pearson RC, Hoover DL, Maples JM. Metabolic flexibility is impaired in women who are pregnant and overweight/obese and related to insulin resistance and inflammation. Metabolism. 2020;104:154142. doi:10.1016/j.metabol.2020.154142.
  • Berry ASF, Pierdon MK, Misic AM, Sullivan MC, O’Brien K, Chen Y, Murray SJ, Ramharack LA, Baldassano RN, Parsons TD, et al. Remodeling of the maternal gut microbiome during pregnancy is shaped by parity. Microbiome. 2021;9(1):146. doi:10.1186/s40168-021-01089-8.
  • Deslypere JP, Van Trappen Y, Thiery M. Influence of parity on plasma lipid levels. Eur J Obstet Gynecol Reprod Biol. 1990;35(1):1–6. doi:10.1016/0028-2243(90)90135-n.
  • Juntunen K. Grand grand multiparity and birth weight. Obstet Gynecol. 1997;90(4):495–499. doi:10.1016/s0029-7844(97)00269-x.
  • Astbury S, Mostyn A, Symonds ME, Bell RC. Nutrient availability, the microbiome, and intestinal transport during pregnancy. Appl Physiol Nutr Metab. 2015;40(11):1100–1106. doi:10.1139/apnm-2015-0117.
  • Bilotta AJ, Ma C, Yang W, Yu Y, Yu Y, Zhao X, Zhou Z, Yao S, Dann SM, Cong Y, et al. Propionate enhances cell speed and persistence to promote intestinal epithelial turnover and repair. Cell Mol Gastroenterol Hepatol. 2021;11(4):1023–1044. doi:10.1016/j.jcmgh.2020.11.011.
  • Tong LC, Wang Y, Wang ZB, Liu WY, Sun S, Li L, Su DF, Zhang LC. Propionate ameliorates dextran Sodium Sulfate-induced colitis by improving intestinal barrier function and reducing inflammation and oxidative stress. Front Pharmacol. 2016;7:253. doi:10.3389/fphar.2016.00253.
  • Ribeiro TA, Breznik JA, Kennedy KM, Yeo E, Kennelly BKE, Jazwiec PA, Patterson VS, Bellissimo CJ, Anhê FF, Schertzer JD, et al. Intestinal permeability and peripheral immune cell composition are altered by pregnancy and adiposity at mid- and late-gestation in the mouse. bioRxiv. 2022;2022.08.20.504644. doi:10.1101/2022.08.20.504644.
  • Vogt JA, Wolever TMS. Fecal acetate is inversely related to acetate absorption from the human rectum and distal colon. J Nutr. 2003;133(10):3145–3148. doi:10.1093/jn/133.10.3145.
  • Szczuko M, Kikut J, Maciejewska D, Kulpa D, Celewicz Z, Ziętek M. The associations of SCFA with anthropometric parameters and carbohydrate metabolism in pregnant women. Int J Mol Sci. 2020;21(23):9212. doi:10.3390/ijms21239212.
  • Chen T, Long W, Zhang C, Liu S, Zhao L, Hamaker BR. Fiber-utilizing capacity varies in prevotella- versus bacteroides-dominated gut microbiota. Sci Rep. 2017;7(1):2594. doi:10.1038/s41598-017-02995-4.
  • Sugino KY, Paneth N, Comstock SS, Rosenfeld CS. Michigan cohorts to determine associations of maternal pre-pregnancy body mass index with pregnancy and infant gastrointestinal microbial communities: late pregnancy and early infancy. PloS One. 2019;14(3):e0213733. doi:10.1371/journal.pone.0213733.
  • Kovatcheva-Datchary P, Nilsson A, Akrami R, Lee YS, De Vadder F, Arora T, Hallen A, Martens E, Björck I, Bäckhed F, et al. Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of prevotella. Cell Metab. 2015;22(6):971–982. doi:10.1016/j.cmet.2015.10.001.
  • Pedersen HK, Gudmundsdottir V, Nielsen HB, Hyotylainen T, Nielsen T, Jensen BAH, Forslund K, Hildebrand F, Prifti E, Falony G, et al. Human gut microbes impact host serum metabolome and insulin sensitivity. Nature. 2016;535(7612):376–381. doi:10.1038/nature18646.
  • Goldstein RF, Abell SK, Ranasinha S, Misso M, Boyle JA, Black MH, Li N, Hu G, Corrado F, Rode L, et al. Association of gestational weight gain with maternal and infant outcomes: a systematic review and meta-analysis. JAMA. 2017;317(21):2207–2225. doi:10.1001/jama.2017.3635.
  • Radulescu L, Munteanu O, Popa F, Cirstoiu M. The implications and consequences of maternal obesity on fetal intrauterine growth restriction. J Med Life. 2013;6(3):292–298. https://www.ncbi.nlm.nih.gov/pubmed/24155784.
  • Enav H, Bäckhed F, Ley RE. The developing infant gut microbiome: a strain-level view. Cell Host & Microbe. 2022;30(5):627–638. doi:10.1016/j.chom.2022.04.009.
  • Müller M, Hernández MAG, Goossens GH, Reijnders D, Holst JJ, Jocken JWE, van Eijk H, Canfora EE, Blaak EE. Circulating but not faecal short-chain fatty acids are related to insulin sensitivity, lipolysis and GLP-1 concentrations in humans. Sci Rep. 2019;9(1):12515. doi:10.1038/s41598-019-48775-0.
  • Atkinson SA, Maran A, Dempsey K, Perreault M, Vanniyasingam T, Phillips SM, Hutton EK, Mottola MF, Wahoush O, Xie F, et al. Be healthy in pregnancy (BHIP): a randomized controlled trial of nutrition and exercise intervention from early pregnancy to achieve recommended gestational weight gain. Nutrients. 2022;14(4):810. doi:10.3390/nu14040810.
  • Whelan FJ, Verschoor CP, Stearns JC, Rossi L, Luinstra K, Loeb M, Smieja M, Johnstone J, Surette MG, Bowdish DME, et al. The loss of topography in the microbial communities of the upper respiratory tract in the elderly. Ann Am Thorac Soc. 2014;11(4):513–521. doi:10.1513/AnnalsATS.201310-351OC.
  • Bartram AK, Lynch MDJ, Stearns JC, Moreno-Hagelsieb G, Neufeld JD. Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end illumina reads. Appl Environ Microbiol. 2011;77(11):3846–3852. doi:10.1128/AEM.02772-10.
  • Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17(1):10–12. doi:10.14806/ej.17.1.200.
  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–583. doi:10.1038/nmeth.3869.
  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41(D1):D590–6. doi:10.1093/nar/gks1219.
  • McMurdie PJ, Holmes S, Watson M. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PloS One. 2013;8(4):e61217. doi:10.1371/journal.pone.0061217.
  • Wickham H. ggplot2: elegant graphics for data analysis. Springer; 2016. https://market.android.com/details?id=book-XgFkDAAAQBAJ.
  • Oksanen J, Simpson G, Blanchet F, Kindt R, Legendre P, Minchin P, O’Hara R, Solymos P, Stevens M, Szoecs, E et al. vegan: community ecology package (R package version 2.6-4). https://CRAN.R-project.org/package=vegan.