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Association of Maternal Roux-en-Y Gastric Bypass with Obstetric Outcomes and Fluid Intelligence in Offspring

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Abstract

Purpose

The purpose of the study is to assess whether Roux-en-Y gastric bypass (RYGB) prior to pregnancy is associated with fluid intelligence in offspring. Additionally, perinatal and obstetric outcomes, and children nutritional status were evaluated.

Material and Methods

Singleton births of women who underwent RYGB between 2000 and 2010 (BS) were matched to two control births by maternal age, delivery year, and gender. Control group 1 (CG1) and control group 2 (CG2) included women with a pre-pregnancy body mass index (BMI) < 35 kg/m2 and ≥ 35 kg/m2, respectively, who had never undergone bariatric surgery.

Results

Thirty-two children from each group (n = 96) were analyzed, mostly female (59%) and Caucasian (82%), with a mean age of 7 ± 2 years. Their general intelligence scores were similar after adjusting for sociodemographic confounders; family economic class was the strongest predictor (low: β = − 20.57; p < 0.001; middle: β = − 9.34; p = 0.019). Gestational diabetes mellitus (OR 0.06; 95% CI 0.03; 0.35) and hypertensive disorders (OR 0.09; 95% CI 0.01; 0.40) were less frequent in BS than CG2. Post-RYGB pregnancies were associated with lower birth weight (P = 0.021) than controls. Child overweight and obesity was higher (OR 4.59; 95% CI 1.55; 13.61; p = 0.006) in CG2 (78%) than CG1 (44%) and similar to BS (65%).

Conclusions

RYGB prior to pregnancy was not associated with fluid intelligence in offspring. Prior RYGB was associated with a lower frequency of gestational diabetes mellitus and hypertensive disorders than in women with a pre-pregnancy BMI ≥ 35 kg/m2, as well as with lower birth weight than both control groups.

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Abbreviations

BMI:

Body mass index

BW:

Birth weight

GA:

Gestational age

GDM:

Gestational diabetes mellitus

GEE:

Generalized estimating equation

GWG:

Gestational weight gain

HPD:

Hypertensive pregnancy disorders

IOM:

Institute of Medicine

LGA:

Large for gestational age

OR:

Odds ratio

RCPM:

Raven’s Colored Progressive Matrices

RPM:

Raven’s Progressive Matrices

RYGB:

Roux-en-Y gastric bypass

SD:

Standard deviation

SE:

Standard error

SGA:

Small for gestational age

WC:

Waist circumference

WHO:

World Health Organization

References

  1. Singh J, Huang CC, Driggers RW, Timofeev J, Amini D, Landy HJ, et al. The impact of pre-pregnancy body mass index on the risk of gestational diabetes. J Matern Fetal Neonatal Med 2012;25(1):5–10.

    Article  Google Scholar 

  2. Aune D, Saugstad OD, Henriksen T, et al. Maternal body mass index and the risk of fetal death, stillbirth, and infant death: a systematic review and meta-analysis. JAMA. 2014;311(15):1536–46.

    Article  CAS  PubMed  Google Scholar 

  3. Stothard KJ, Tennant PW, Bell R, et al. Maternal overweight and obesity and the risk of congenital anomalies: a systematic review and meta-analysis. JAMA. 2009;301(6):636–50.

    Article  CAS  PubMed  Google Scholar 

  4. McDonald SD, Han Z, Mulla S, et al. Overweight and obesity in mothers and risk of preterm birth and low birth weight infants: systematic review and meta-analyses. BMJ. 2010;341:c3428.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Bilano VL, Ota E, Ganchimeg T, et al. Risk factors of pre-eclampsia/eclampsia and its adverse outcomes in low- and middle-income countries: a WHO secondary analysis. PLoS One. 2014;9(3):e91198.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Shankar K, Harrell A, Liu X, et al. Maternal obesity at conception programs obesity in the offspring. Am J Physiol Regul Integr Comp Physiol. 2008;294(2):R528–38.

    Article  CAS  PubMed  Google Scholar 

  7. Borengasser SJ, Lau F, Kang P, Blackburn ML, Ronis MJ, Badger TM, et al. Maternal obesity during gestation impairs fatty acid oxidation and mitochondrial SIRT3 expression in rat offspring at weaning. PLoS One 2011;6(8):e24068.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Basu S, Haghiac M, Surace P, Challier JC, Guerre-Millo M, Singh K, et al. Pregravid obesity associates with increased maternal endotoxemia and metabolic inflammation. Obesity (Silver Spring) 2011;19(3):476–482.

    Article  CAS  PubMed  Google Scholar 

  9. Stewart FM, Freeman DJ, Ramsay JE, et al. Longitudinal assessment of maternal endothelial function and markers of inflammation and placental function throughout pregnancy in lean and obese mothers. J Clin Endocrinol Metab. 2007;92(3):969–75.

    Article  CAS  PubMed  Google Scholar 

  10. Aye IL, Lager S, Ramirez VI, Gaccioli F, Dudley DJ, Jansson T, et al. Increasing maternal body mass index is associated with systemic inflammation in the mother and the activation of distinct placental inflammatory pathways. Biol Reprod 2014;90(6):129.

  11. Basatemur E, Gardiner J, Williams C, et al. Maternal prepregnancy BMI and child cognition: a longitudinal cohort study. Pediatrics. 2013;131(1):56–63.

    Article  PubMed  Google Scholar 

  12. Hinkle SN, Schieve LA, Stein AD, et al. Associations between maternal prepregnancy body mass index and child neurodevelopment at 2 years of age. Int J Obes. 2012;36(10):1312–9.

    Article  CAS  Google Scholar 

  13. Adane AA, Mishra GD, Tooth LR. Maternal pre-pregnancy obesity and childhood physical and cognitive development of children: a systematic review. Int J Obes. 2016;40(11):1608–18.

    Article  CAS  Google Scholar 

  14. Alosco ML, Stanek KM, Galioto R, Korgaonkar MS, Grieve SM, Brickman AM, et al. Body mass index and brain structure in healthy children and adolescents. Int J Neurosci 2014;124(1):49–55.

    Article  PubMed  Google Scholar 

  15. Ou X, Thakali KM, Shankar K, et al. Maternal adiposity negatively influences infant brain white matter development. Obesity (Silver Spring). 2015;23(5):1047–54.

    Article  CAS  Google Scholar 

  16. Li JF, Lai DD, Lin ZH, et al. Comparison of the long-term results of Roux-en-Y gastric bypass and sleeve gastrectomy for morbid obesity: a systematic review and meta-analysis of randomized and nonrandomized trials. Surg Laparosc Endosc Percutan Tech. 2014;24(1):1–11.

    Article  PubMed  Google Scholar 

  17. Maggard MA, Yermilov I, Li Z, Maglione M, Newberry S, Suttorp M, et al. Pregnancy and fertility following bariatric surgery: a systematic review. JAMA 2008;300(19):2286–2296.

    Article  CAS  PubMed  Google Scholar 

  18. Roos N, Neovius M, Cnattingius S, Trolle Lagerros Y, Sääf M, Granath F, et al. Perinatal outcomes after bariatric surgery: nationwide population based matched cohort study. BMJ 2013;347:f6460.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Galazis N, Docheva N, Simillis C, et al. Maternal and neonatal outcomes in women undergoing bariatric surgery: a systematic review and meta-analysis. Eur J Obstet Gynecol Reprod Biol. 2014;181:45–53.

    Article  PubMed  Google Scholar 

  20. Johansson K, Stephansson O, Neovius M. Outcomes of pregnancy after bariatric surgery. N Engl J Med. 2015;372(23):2267.

    CAS  PubMed  Google Scholar 

  21. Yousseif A, Emmanuel J, Karra E, Millet Q, Elkalaawy M, Jenkinson AD, et al. Differential effects of laparoscopic sleeve gastrectomy and laparoscopic gastric bypass on appetite, circulating acyl-ghrelin, peptide YY3-36 and active GLP-1 levels in non-diabetic humans. Obes Surg 2014;24(2):241–252.

    Article  PubMed Central  Google Scholar 

  22. Salehi M, Prigeon RL, D'Alessio DA. Gastric bypass surgery enhances glucagon-like peptide 1-stimulated postprandial insulin secretion in humans. Diabetes. 2011;60(9):2308–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Jans G, Matthys C, Bogaerts A, Lannoo M, Verhaeghe J, Van der Schueren B, et al. Maternal micronutrient deficiencies and related adverse neonatal outcomes after bariatric surgery: a systematic review. Adv Nutr 2015;6(4):420–429.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Gadgil MD, Chang HY, Richards TM, Gudzune KA, Huizinga MM, Clark JM, et al. Laboratory testing for and diagnosis of nutritional deficiencies in pregnancy before and after bariatric surgery. J Women’s Health (Larchmt) 2014;23(2):129–137.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Veena SR, Gale CR, Krishnaveni GV, et al. Association between maternal nutritional status in pregnancy and offspring cognitive function during childhood and adolescence; a systematic review. BMC Pregnancy Childbirth. 2016;16:220.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Associação Brasileira de Empresas de Pesquisa (ABEP). Critério de classificação econômica Brasil. São Paulo: ABEP; 2014.

  27. Institute of Medicine, National Research Council (IOM/NRC), 2009. Weight gain during pregnancy: reexaminig the guidelines. Rasmussen KM and Yaktine AL.

  28. Villar J, Cheikh Ismail L, Victora CG, Ohuma EO, Bertino E, Altman DG, et al. International standards for newborn weight, length, and head circumference by gestational age and sex: the newborn cross-sectional study of the INTERGROWTH-21st project. Lancet 2014;384(9946):857–868.

    Article  Google Scholar 

  29. Fernández JR, Redden DT, Pietrobelli A, et al. Waist circumference percentiles in nationally representative samples of African-American, European-American, and Mexican-American children and adolescents. J Pediatr. 2004;145(4):439–44.

    Article  PubMed  Google Scholar 

  30. Raven J, Raven JC, Court JH. Manual for Raven’s progressive matrices and vocabulary scales. Section 2: the coloured progressive matrices: introducing the parallel version of the test. London: Oxford Psychologist Press Ltd; 1998.

    Google Scholar 

  31. Raven J, Raven JC, Court JH. Manual for Raven’s progressive matrices and vocabulary scales. Section 3: standard progressive matrices (including the parallel and plus versions of the tests). Standard progressive matrices: sets A, B, C, D and E. London: Oxford Psychologist Press Ltd; 1998.

    Google Scholar 

  32. Raven J. The Raven’s progressive matrices: change and stability over culture and time. Cogn Psychol. 2000;41(1):1–48.

    Article  CAS  PubMed  Google Scholar 

  33. Mackintosh NJ, Bennett ES. What do Raven’s matrices measure? An analysis in terms of sex differences. Intelligence. 2005;33(6):663–74.

    Article  Google Scholar 

  34. de Onis M, Onyango AW, Borghi E, et al. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ. 2007;85(9):660–7.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Dell’Agnolo CM, Cyr C, de Montigny F, et al. Pregnancy after bariatric surgery: obstetric and perinatal outcomes and the growth and development of children. Obes Surg. 2015;25(11):2030–9.

    Article  PubMed  Google Scholar 

  36. Merikangas KR, He JP, Brody D, et al. Prevalence and treatment of mental disorders among US children in the 2001-2004 NHANES. Pediatrics. 2010;125(1):75–81.

    Article  PubMed  Google Scholar 

  37. Hurt H, Betancourt LM. Effect of socioeconomic status disparity on child language and neural outcome: how early is early? Pediatr Res. 2016;79(1–2):148–58.

    Article  PubMed  Google Scholar 

  38. Sheridan MA, Sarsour K, Jutte D, et al. The impact of social disparity on prefrontal function in childhood. PLoS One. 2012;7(4):e35744.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Luby J, Belden A, Botteron K, Marrus N, Harms MP, Babb C, et al. The effects of poverty on childhood brain development: the mediating effect of caregiving and stressful life events. JAMA Pediatr 2013;167(12):1135–1142.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Godfrey KM, Reynolds RM, Prescott SL, Nyirenda M, Jaddoe VW, Eriksson JG, et al. Influence of maternal obesity on the long-term health of offspring. Lancet Diabetes Endocrinol 2017;5(1):53–64.

    Article  Google Scholar 

  41. Victora CG, Horta BL, Loret de Mola C, Quevedo L, Pinheiro RT, Gigante DP, et al. Association between breastfeeding and intelligence, educational attainment, and income at 30 years of age: a prospective birth cohort study from Brazil. Lancet Glob Health 2015;3(4):e199–e205.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Horta BL, Loret de Mola C, Victora CG. Breastfeeding and intelligence: a systematic review and meta-analysis. Acta Paediatr. 2015;104(467):14–9.

    Article  PubMed  Google Scholar 

  43. Weintraub AY, Levy A, Levi I, et al. Effect of bariatric surgery on pregnancy outcome. Int J Gynaecol Obstet. 2008;103(3):246–51.

    Article  PubMed  Google Scholar 

  44. Yu ZB, Han SP, Zhu GZ, et al. Birth weight and subsequent risk of obesity: a systematic review and meta-analysis. Obes Rev. 2011;12(7):525–42.

    Article  CAS  PubMed  Google Scholar 

  45. Jornayvaz FR, Vollenweider P, Bochud M, et al. Low birth weight leads to obesity, diabetes and increased leptin levels in adults: the CoLaus study. Cardiovasc Diabetol. 2016;15:73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Kral JG, Biron S, Simard S, Hould FS, Lebel S, Marceau S, et al. Large maternal weight loss from obesity surgery prevents transmission of obesity to children who were followed for 2 to 18 years. Pediatrics 2006;118(6):e1644–e1649.

    Article  PubMed  Google Scholar 

  47. Willmer M, Berglind D, Sørensen TI, et al. Surgically induced interpregnancy weight loss and prevalence of overweight and obesity in offspring. PLoS One. 2013;8(12):e82247.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Polderman TJ, Benyamin B, de Leeuw CA, Sullivan PF, van Bochoven A, Visscher PM, et al. Meta-analysis of the heritability of human traits based on fifty years of twin studies. Nat Genet 2015;47(7):702–709.

    Article  CAS  PubMed  Google Scholar 

  49. Larjani S, Spivak I, Hao Guo M, Aliarzadeh B, Wang W, Robinson S, et al. Preoperative predictors of adherence to multidisciplinary follow-up care postbariatric surgery. Surg Obes Relat Dis 2016;12(2):350–356.

    Article  PubMed  Google Scholar 

  50. Khorgami Z, Zhang C, Messiah SE, de la Cruz-Muñoz N. Predictors of postoperative aftercare attrition among gastric bypass patients. Bariatr Surg Pract Patient Care 2015;10(2):79–83.

    Article  PubMed  PubMed Central  Google Scholar 

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Funding Sources

The study was funded by the Fundo de Incentivo à Pesquisa e Eventos (FIPE) of the Hospital de Clínicas de Porto Alegre and the National Council of Technological and Scientific Development (CNPq).

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Correspondence to Carina Andriatta Blume.

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The authors declare that they have no conflicts of interest.

Ethical Approval

The study was performed according to the principles of the Helsinki Declaration. The HCPA and HSLPUCRS Ethics Committees approved the study protocol.

Informed Consent

Informed consent was obtained from all individual participants included in the study.

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Blume, C.A., Machado, B.M., da Rosa, R.R. et al. Association of Maternal Roux-en-Y Gastric Bypass with Obstetric Outcomes and Fluid Intelligence in Offspring. OBES SURG 28, 3611–3620 (2018). https://doi.org/10.1007/s11695-018-3407-5

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  • DOI: https://doi.org/10.1007/s11695-018-3407-5

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