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Maternal intake of omega-3 and omega-6 polyunsaturated fatty acids during mid-pregnancy is inversely associated with linear growth

Part of: DOHaD on International Women's Day 2020 French DOHaD

Published online by Cambridge University Press:  18 April 2018

M. Al-Hinai ,
A. Baylin ,
M. M. Tellez-Rojo ,
A. Cantoral ,
A. Ettinger ,
M. Solano-González ,
K. E. Peterson  and
W. Perng
M. Al-Hinai
Affiliation:
Department of Nutritional Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA Department of Food Science and Human Nutrition, Sultan Qaboos University College of Agriculture and Marine Science, Muscat, Oman
A. Baylin
Affiliation:
Department of Nutritional Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, MI, USA
M. M. Tellez-Rojo
Affiliation:
Center for Nutrition and Health Research, National Institute of Public Health, Mexico City, MX, USA
A. Cantoral
Affiliation:
Center for Nutrition and Health Research, National Institute of Public Health, Mexico City, MX, USA
A. Ettinger
Affiliation:
Department of Nutritional Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA
M. Solano-González
Affiliation:
Center for Nutrition and Health Research, National Institute of Public Health, Mexico City, MX, USA
K. E. Peterson
Affiliation:
Department of Nutritional Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA Center for Human Growth and Development, University of Michigan, Ann Arbor, MI, USA
W. Perng*
Affiliation:
Department of Nutritional Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, MI, USA
*
Address for correspondence: W. Perng, Department of Nutritional Sciences, University of Michigan School of Public Health, 1415, Washington Heights, Room 1860 SPH 1, Ann Arbor, MI 48109-2029, USA. E-mail: perngwei@umich.edu
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Abstract

This study investigates relations of maternal N-3 and N-6 polyunsaturated fatty acids (PUFA) intake during pregnancy with offspring body mass index (BMI), height z-score and metabolic risk (fasting glucose, C-peptide, leptin, lipid profile) during peripuberty (8–14 years) among 236 mother–child pairs in Mexico. We used food frequency questionnaire data to quantify trimester-specific intake of N-3 alpha-linolenic acid, eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA); N-6 linoleic acid and arachidonic acid (AA); and N-6:N-3 (AA:EPA+DHA), which accounts for the fact that the two PUFA families have opposing effects on physiology. Next, we used multivariable linear regression models that accounted for maternal education and parity, and child’s age, sex and pubertal status, to examine associations of PUFA intake with the offspring outcomes. In models where BMI z-score was the outcome, we also adjusted for height z-score. We found that higher second trimester intake of EPA, DHA and AA were associated with lower offspring BMI and height z-score. For example, each 1-s.d. increment in second trimester EPA intake corresponded with 0.25 (95% CI: 0.03, 0.47) z-scores lower BMI and 0.20 (0.05, 0.36) z-scores lower height. Accounting for height z-score in models where BMI z-score was the outcome attenuated estimates [e.g., EPA: −0.16 (−0.37, 0.05)], suggesting that this relationship was driven by slower linear growth rather than excess adiposity. Maternal PUFA intake was not associated with the offspring metabolic biomarkers. Our findings suggest that higher PUFA intake during mid-pregnancy is associated with lower attained height in offspring during peripuberty. Additional research is needed to elucidate mechanisms and to confirm findings in other populations.

Keywords

adipositymetabolic riskomega-3 (N-3)omega-6 (N-6)peripuberty
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 9 , Issue 4: Themed Issue: French DOHaD , August 2018 , pp. 432 - 441
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

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References

1. Wiktorowska-Owczarek, A, Bereziska, M, Nowak, JZ. PUFAs: structures, metabolism and functions. Adv Clin Exp Med. 2015; 24, 931–941.Google Scholar
2. Van Vlies, N, Hogenkamp, A, Fear, AL, et al. Perinatal programming of murine immune responses by polyunsaturated fatty acids. J Dev Orig Health Dis. 2011; 2, 112–123.Google Scholar
3. Muhlhausler, BS, Ailhaud, GP. Omega-6 polyunsaturated fatty acids and the early origins of obesity. Curr Opin Endocrinol Diabetes Obes. 2013; 20, 56–61.Google Scholar
4. Perng, W, Oken, E. Programming long term health: maternal and fetal nutritional and dietary needs. In Early Nutrition and Long-Term Health: Mechanisms, Consequences and Opportunities (ed. Saavedra JM), 2017; pp. 375–411. Oxford University Press: Duxford, England.Google Scholar
5. Mennitti, LV, Oliveira, JL, Morais, CA, et al. Type of fatty acids in maternal diets during pregnancy and/or lactation and metabolic consequences of the offspring. J Nutr Biochem. 2015; 26, 99–111.Google Scholar
6. Wadhwa, PD, Buss, C, Entringer, S, Swanson, JM, Ph, D. Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med. 2010; 27, 358–368.Google Scholar
7. Korotkova, M, Gabrielsson, B, Lönn, M, Hanson, L-Å, Strandvik, B. Leptin levels in rat offspring are modified by the ratio of linoleic to α-linolenic acid in the maternal diet. J Lipid Res. 2002; 43, 1743–1749.Google Scholar
8. Korotkova, M, Gabrielsson, BG, Holma, A, et al. Gender-related long-term effects in adult rats by perinatal dietary ratio of n-6/n-3 fatty acids. Am J Physiol Regul Integr Comp Physiol. 2005; 288, 575–579.Google Scholar
9. Heerwagen, MJR, Stewart, MS, de la Houssaye, BA, Janssen, RC, Friedman, JE. Transgenic increase in N-3/N-6 fatty acid ratio reduces maternal obesity-associated inflammation and limits adverse developmental programming in mice. PLoS One. 2013; 8, e67791.Google Scholar
10. Schmitz, G, Ecker, J. The opposing effects of n-3 and n-6 fatty acids. Prog Lipid Res. 2008; 47, 147–155.Google Scholar
11. Madsen, L, Petersen, RK, Kristiansen, K. Regulation of adipocyte differentiation and function by polyunsaturated fatty acids. Biochim Biophys Acta. 2005; 1740, 266–286.Google Scholar
12. Ailhaud, G, Guesnet, P. Fatty acid composition of fats is an early determinant of childhood obesity: a short review and an opinion. Obes Rev. 2004; 5, 21–26.Google Scholar
13. Donahue, SMA, Rifas-Shiman, SL, Gold, DR, et al. Prenatal fatty acid status and child adiposity at age 3 y: results from a US pregnancy cohort. Am J Clin Nutr. 2011; 93, 780–788.Google Scholar
14. De Vries, PS, Gielen, M, Rizopoulos, D, et al. Association between polyunsaturated fatty acid concentrations in maternal plasma phospholipids during pregnancy and offspring adiposity at age 7: the MEFAB cohort. Prostaglandins Leukot Essent Fat Acids. 2014; 91, 81–85.Google Scholar
15. Vidakovic, A, Santos, S, Williams, MA, et al. Maternal plasma n-3 and n-6 polyunsaturated fatty acid concentrations during pregnancy and subcutaneous fat mass in infancy. Obesity. 2016; 24, 1759–1766.Google Scholar
16. Hakola, L, Takkinen, H-M, Niinistö, S, et al. Maternal fatty acid intake during pregnancy and the development of childhood overweight: a birth cohort study. Pediatr Obes. 2016; 12, 1–12.Google Scholar
17. Instituto Nacional de Salud Publica. Encuesta Nacional de Salud y Nutricion. Instituto Nacional de Salud Publica, 2016.Google Scholar
18. Hernández-Avila, M, Romieu, I, Parra, S, et al. Validity and reproducibility of a food frequency questionnaire to assess dietary intake of women living in Mexico City. Salud Publica Mex. 1998; 40, 133–140.Google Scholar
19. Willett, W. Implications of total energy intake for epidemiologic analyses. In Nutritional Epidemiology (ed. Walter W). 2nd edn, 1998; pp. 279–298. Oxford University Press: New York.Google Scholar
20. De Onis, M, Onyango, AW, Borghi, E, et al. Development of a WHO growth reference for school-aged children and adolescents. Bull World Heal Organ. 2007; 85, 812–819.Google Scholar
21. Perng, W, Fernandez, C, Peterson, KE, et al. Dietary patterns exhibit sex-specific associations with adiposity and metabolic risk in a cross-sectional study in urban Mexican adolescents. J Nutr. 2017; 10, 1977–1985.Google Scholar
22. Bonser, AM, Garcia-Webb, P, Harrison, LC. C-peptide measurement: methods and clinical utility. Crit Rev Clin Lab Sci. 1984; 19, 297–352.Google Scholar
23. 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; 18, 499–502.Google Scholar
24. Viitasalo, A, Lakka, TA, Laaksonen, DE, et al. Validation of metabolic syndrome score by confirmatory factor analysis in children and adults and prediction of cardiometabolic outcomes in adults. Diabetologia. 2014; 57, 940–949.Google Scholar
25. Perng, W, Hector, EC, Song, PXK, et al. Metabolomic determinants of metabolic risk in Mexican adolescents. Obesity. 2017; 25, 1594–1602.Google Scholar
26. Shi, P, Goodson, JM, Hartman, ML, et al. Continuous metabolic syndrome scores for children using salivary biomarkers. PLoS One. 2015; 10, 1–16.Google Scholar
27. Hernández, B, Gortmaker, SL, Colditz, GA, Peterson, KE, Laird, NMP-CS. Association of obesity with physical activity, television programs and other forms of video viewing among children in Mexico city. Int J Obes Relat Metab Disord. 1999; 23, 845–854.Google Scholar
28. Hernández, B, Gortmaker, SL, Laird, NM, Colditz, GA, Parra-Cabrera, SPK. Validity and reproducibility of a questionnaire on physical activity and non-activity for school children in Mexico City. Salud Publica Mex. 2000; 42, 315–323.Google Scholar
29. Chavarro, JE, Watkins, DJ, Afeiche, MC, et al. Validity of self-assessed sexual maturation against physician assessments and hormone levels. J Pediatr. 2017; 186, 172–178.e3.Google Scholar
30. Marshall, WA, Tanner, JM. Variations in the pattern of pubertal changes in boys. Arch Dis Child. 1970; 45, 13–23.Google Scholar
31. Eide, MG, Øyen, N, Skjærven, R, et al. Size at birth and gestational age as predictors of adult height and weight. Epidemiology. 2005; 16, 175–181.Google Scholar
32. Carlsen, K, Pedersen, L, Bønnelykke, K, et al. Association between whole-blood polyunsaturated fatty acids in pregnant women and early fetal weight. Eur J Clin Nutr. 2013; 67, 978–983.Google Scholar
33. Watkins, B. Bioactive fatty acids: role in bone biology and bone cell function. Prog Lipid Res. 2001; 40, 125–148.Google Scholar
34. Lau, BYY, Cohen, DJA, Ward, WE, Ma, DWL. Investigating the role of polyunsaturated fatty acids in bone development using animal models. Molecules. 2013; 18, 14203–14227.Google Scholar
35. Koren, N, Simsa-Maziel, S, Shahar, R, Schwartz, B, Monsonego-Ornan, E. Exposure to omega-3 fatty acids at early age accelerate bone growth and improve bone quality. J Nutr Biochem. 2014; 25, 623–633.Google Scholar
36. Salari, P, Rezaie, A, Larijani, B, Abdollahi, M. A systematic review of the impact of n-3 fatty acids in bone health and osteoporosis. Med Sci Monit. 2008; 14, RA37–RA44.Google Scholar
37. Basu, N, Tutino, R, Zhang, Z, et al. Mercury levels in pregnant women, children, and seafood from Mexico City. Environ Res. 2014; 135, 63–69.Google Scholar
38. Cantoral, A, Batis, C, Basu, N. National estimation of seafood consumption in Mexico: implications for exposure to methylmercury and polyunsaturated fatty acids. Chemosphere. 2017; 174, 289–296.Google Scholar
39. Murcia, M, Ballester, F, Enning, AM, Iniguez, C, et al. Prenatal mercury exposure and birth outcomes. Environ Res. 2016; 151, 11–20.Google Scholar
40. Hyde, NK, Brennan-Olsen, SL, Wark, JD, Hosking, SM, Pasco, JA. Maternal dietary nutrient intake during pregnancy and offspring linear growth and bone: the vitamin D in pregnancy cohort study. Calcif Tissue Int. 2016; 100, 1–8.Google Scholar
41. Hwang, J, Lee, J, Kim, K-N, et al. Maternal iron intake at mid-pregnancy is associated with reduced fetal growth: results from Mothers and Children’s Environmental Health (MOCEH) study. Nutr J. 2013; 12, 38.Google Scholar
42. Borazjani, F, Angali, KA, Kulkarni, SS. Milk and protein intake by pregnant women affects growth of foetus. J Heal Popul Nutr. 2013; 31, 435–445.Google Scholar
43. Lise Brantsæter, A, Olafsdottir, A, Forsum, E, Olsen, S, Thorsdottir, I. Does milk and dairy consumption during pregnancy influence fetal growth and infant birthweight? A systematic literature review. Food Nutr Res. 2012; 56, 20050.Google Scholar
44. Tanner, JM. Fetus into Man: Physical Growth from Conception to Maturity. Revised ed, 1990. Library of Congress Cataloging-in-Publication Data. Cambridge, MA.Google Scholar
45. Much, D, Brunner, S, Vollhardt, C, et al. Effect of dietary intervention to reduce the n-6/n-3 fatty acid ratio on maternal and fetal fatty acid profile and its relation to offspring growth and body composition at 1 year of age. Eur J Clin Nutr. 2013; 67, 282–288.Google Scholar
46. Labarthe, DR, Nichaman, MZ, Harrist, RB, Grunbaum, JA, Dai, S. Development of cardiovascular risk factors from ages 8 to 18 in project HeartBeat! Circulation. 1997; 95, 2636–2642.Google Scholar
47. Dai, S, Fulton, JE, Harrist, RB, et al. Blood lipids in children: age-related patterns and association with body-fat indices project HeartBeat! Am J Prev Med. 2009; 37, S56–S64.Google Scholar
48. Goran, MI, Gower, BA. Longitudinal study on pubertal insulin resistance. Diabetes. 2001; 50, 2444–2450.Google Scholar
49. Lee, JM. Why young adults hold the key to assessing the obesity epidemic in children. Arch Pediatr Adolesc Med. 2008; 162, 682–687.Google Scholar
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