Effects of breastfeeding on reducing the risk of overweight and obesity among offspring exposed to intrauterine hyperglycemia: a meta-analysis_Chinese Journal of Evidence-Based Medicine

Authors：

CAO Yidan ^1,2,3 , GONG Kexin ^1,2,3 ,  ZHU Beibei ^1,2,3 , TAO Fangbiao ^1,2,3

1. Department of Maternal, Child and Adolescent Health, School of Public Health, Anhui Medical University, Hefei 230032, P. R. China;
2. Key Laboratory of Population Health Across Life Cycle (Anhui Medical University), Ministry of Education of the People’s Republic of China, Hefei 230032, P. R. China;
3. Anhui Provincial Key Laboratory of Population Health and Aristogenics, Hefei 230032, P. R. China;

Corresponding author：

ZHU Beibei, Email: a513275541@126.com

Keywords：

Intrauterine hyperglycemia; Breastfeeding; Offspring overweight or obesity; Observational study; Meta-analysis

DOI：

10.7507/1672-2531.202203128

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To systematically review the effectiveness of breastfeeding duration and intensity in reducing the risk of overweight or obesity among offspring exposed to intrauterine hyperglycemia. Methods The PubMed, EMbase, Web of Science, CBM, WanFang Data, CNKI and VIP databases were electronically searched to collect observational studies on the associations of breastfeeding with the risk of overweight or obesity among offspring exposed to intrauterine hyperglycemia from inception to September 25^th, 2021. Two reviewers independently screened the literature, extracted data and assessed the risk of bias of the included studies. Stata 16.0 software was used for the meta-analysis. Results A total of 12 657 participants from 13 observational studies were included. The results of meta-analysis showed that breastfeeding could reduce the risk of overweight or obesity among offspring exposed to intrauterine hyperglycemia (OR=0.67, 95%CI 0.53 to 0.84, P=0.001). Subgroup analysis revealed a protective effect of breastfeeding for both 1-6 months (OR=0.53, 95%CI 0.37 to 0.75, P<0.001) and ≥6 months (OR=0.56, 95%CI 0.46 to 0.69, P<0.001); however, breastfeeding shorter than one month was suggested to increase the risk of overweight or obesity (OR=2.15, 95%CI 1.41 to 3.27, P<0.001). Conclusion Available evidence suggests that breastfeeding for more than one month is effective in reducing the risk of overweight or obesity in offspring exposed to intrauterine hyperglycemia, and women with hyperglycemia should be encouraged to breastfeed their offspring for at least 1 month to achieve the effect. Due to the limited quantity and quality of the included studies, more high-quality studies are needed to verify the above conclusion.

Citation： CAO Yidan, GONG Kexin, ZHU Beibei, TAO Fangbiao. Effects of breastfeeding on reducing the risk of overweight and obesity among offspring exposed to intrauterine hyperglycemia: a meta-analysis. Chinese Journal of Evidence-Based Medicine, 2022, 22(10): 1167-1174. doi: 10.7507/1672-2531.202203128 Copy

1.	李玲. 妊娠期高血糖人群的类型和管理策略. 中华医学信息导报, 2021, 36(10): 12.
2.	Silverman BL, Rizzo T, Green OC, et al. Long-term prospective evaluation of offspring of diabetic mothers. Diabetes, 1991, 40(Suppl 2): 121-125.
3.	Buchanan TA, Xiang AH, Page KA. Gestational diabetes mellitus: risks and management during and after pregnancy. Nat Rev Endocrinol, 2012, 8(11): 639-649.
4.	Woo JG, Martin LJ. Does breastfeeding protect against childhood obesity. Moving beyond observational evidence. Curr Obes Rep, 2015, 4(2): 207-216.
5.	Cope MB, Allison DB. Critical review of the World Health Organization's (WHO) 2007 report on 'evidence of the long-term effects of breastfeeding: systematic reviews and meta-analysis' with respect to obesity. Obes Rev, 2008, 9(6): 594-605.
6.	Weng SF, Redsell SA, Swift JA, et al. Systematic review and meta-analyses of risk factors for childhood overweight identifiable during infancy. Arch Dis Child, 2012, 97(12): 1019-1026.
7.	Fenger-Grøn J, Fenger-Grøn M, Blunck CH, et al. Low breastfeeding rates and body mass index in Danish children of women with gestational diabetes mellitus. Int Breastfeed J, 2015, 10: 26.
8.	Hui LL, Li AM, Nelson EAS, et al. In utero exposure to gestational diabetes and adiposity: does breastfeeding make a difference. Int J Obes (Lond), 2018, 42(7): 1317-1325.
9.	Matias SL, Dewey KG, Quesenberry CP, et al. Maternal prepregnancy obesity and insulin treatment during pregnancy are independently associated with delayed lactogenesis in women with recent gestational diabetes mellitus. Am J Clin Nutr, 2014, 99(1): 115-121.
10.	Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
11.	Higgins JPT, Thomas J, Chandler J, et al. Cochrane handbook for systematic reviews of interventions. 2nd Edition. Chichester (UK): John Wiley & Sons, 2019.
12.	赵亚玲, 马润玫, 黄永坤, 等. 母乳喂养对妊娠期糖尿病母亲子代儿童期超重的影响. 中国当代儿科杂志, 2013, 15(1): 56-61.
13.	Schaefer-Graf UM, Hartmann R, Pawliczak J, et al. Association of breast-feeding and early childhood overweight in children from mothers with gestational diabetes mellitus. Diabetes Care, 2006, 29(5): 1105-1107.
14.	Huvinen E, Tuomaala AK, Bergman PH, et al. Ascending growth is associated with offspring adiposity in pregnancies complicated with obesity or gestational diabetes. J Clin Endocrinol Metab, 2021, 106(5): e1993-e2004.
15.	Mayer-Davis EJ, Rifas-Shiman SL, Zhou L, et al. Breast-feeding and risk for childhood obesity: does maternal diabetes or obesity status matter. Diabetes Care, 2006, 29(10): 2231-2237.
16.	Vandyousefi S, Whaley SE, Widen EM, et al. Association of breastfeeding and early exposure to sugar-sweetened beverages with obesity prevalence in offspring born to mothers with and without gestational diabetes mellitus. Pediatr Obes, 2019, 14(12): e12569.
17.	Faith MS, Hittner JB, Hurston SR, et al. Association of infant temperament with subsequent obesity in young children of mothers with gestational diabetes mellitus. JAMA Pediatr, 2019, 173(5): 424-433.
18.	Plagemann A, Harder T, Franke K, et al. Long-term impact of neonatal breast-feeding on body weight and glucose tolerance in children of diabetic mothers. Diabetes Care, 2002, 25(1): 16-22.
19.	Rodekamp E, Harder T, Kohlhoff R, et al. Long-term impact of breast-feeding on body weight and glucose tolerance in children of diabetic mothers: role of the late neonatal period and early infancy. Diabetes Care, 2005, 28(6): 1457-1462.
20.	Zhao YL, Ma RM, Lao TT, et al. Maternal gestational diabetes mellitus and overweight and obesity in offspring: a study in Chinese children. J Dev Orig Health Dis, 2015, 6(6): 479-484.
21.	Kaul P, Bowker SL, Savu A, et al. Association between maternal diabetes, being large for gestational age and breast-feeding on being overweight or obese in childhood. Diabetologia, 2019, 62(2): 249-258.
22.	Hummel S, Weiß A, Bonifacio E, et al. Associations of breastfeeding with childhood autoimmunity, allergies, and overweight: The Environmental Determinants of Diabetes in the Young (TEDDY) study. Am J Clin Nutr, 2021, 114(1): 134-142.
23.	Hummel S, Pflüger M, Kreichauf S, et al. Predictors of overweight during childhood in offspring of parents with type 1 diabetes. Diabetes Care, 2009, 32(5): 921-925.
24.	Feig DS, Lipscombe LL, Tomlinson G, et al. Breastfeeding predicts the risk of childhood obesity in a multi-ethnic cohort of women with diabetes. J Matern Fetal Neonatal Med, 2011, 24(3): 511-515.
25.	Birch LL, Fisher JO. Development of eating behaviors among children and adolescents. Pediatrics. 1998, 101(3 Pt 2): 539-549.
26.	Lucas A, Boyes S, Bloom SR, et al. Metabolic and endocrine responses to a milk feed in six-day-old term infants: differences between breast and cow's milk formula feeding. Acta Paediatr Scand, 1981, 70(2): 195-200.
27.	Lucas A, Sarson DL, Blackburn AM, et al. Breast vs bottle: endocrine responses are different with formula feeding. Lancet, 1980, 1(8181): 1267-1269.
28.	Weber M, Grote V, Closa-Monasterolo R, et al. Lower protein content in infant formula reduces BMI and obesity risk at school age: follow-up of a randomized trial. Am J Clin Nutr, 2014, 99(5): 1041-1051.
29.	Assunção ML, Ferreira HS, Coutinho SB, et al. Protective effect of breastfeeding against overweight can be detected as early as the second year of life: a study of children from one of the most socially-deprived areas of Brazil. J Health Popul Nutr, 2015, 33(1): 85-91.
30.	Zheng JS, Liu H, Li J, et al. Exclusive breastfeeding is inversely associated with risk of childhood overweight in a large Chinese cohort. J Nutr, 2014, 144(9): 1454-1459.
31.	叶慧. 妊娠期糖尿病对产后不同泌乳阶段母乳营养成分及微生物多样性影响研究. 福州: 福建医科大学, 2021.
32.	Qiao J, Dai LJ, Zhang Q, et al. A meta-analysis of the association between breastfeeding and early childhood obesity. J Pediatr Nurs, 2020, 53: 57-66.
33.	许金婷. 妊娠期糖尿病对婴幼儿肥胖的影响. 济南: 山东大学, 2018.
34.	Gillman MW, Rifas-Shiman SL, Camargo CA, et al. Risk of overweight among adolescents who were breastfed as infants. JAMA, 2001, 285(19): 2461-2467.
35.	Harder T, Bergmann R, Kallischnigg G, et al. Duration of breastfeeding and risk of overweight: a meta-analysis. Am J Epidemiol, 2005, 162(5): 397-403.
36.	Dror DK, Allen LH. Retinol-to-fat ratio and retinol concentration in human milk show similar time trends and associations with maternal factors at the population level: a systematic review and meta-analysis. Adv Nutr, 2018, 9(suppl_1): 332S-346S.
37.	Stettler N, Stallings VA, Troxel AB, et al. Weight gain in the first week of life and overweight in adulthood: a cohort study of European American subjects fed infant formula. Circulation, 2005, 111(15): 1897-1903.
38.	Anderson SE, Keim SA. Parent-child interaction, self-regulation, and obesity prevention in early childhood. Curr Obes Rep, 2016, 5(2): 192-200.
39.	齐芮宁, 李立梅, 陈静. 国内外妊娠期糖尿病产妇母乳喂养影响因素及促进措施的研究进展. 中华现代护理杂志, 2019, 25(20): 2632-2636.
40.	张绍敏. 产后不同阶段妊娠糖尿病产妇母乳喂养状况及影响因素研究. 中国妇幼保健, 2015, 30(33): 5765-5767.
41.	Jagiello KP, Azulay Chertok IR. Women's experiences with early breastfeeding after gestational diabetes. J Obstet Gynecol Neonatal Nurs, 2015, 44(4): 500-509.
42.	Hilson JA, Rasmussen KM, Kjolhede CL. High prepregnant body mass index is associated with poor lactation outcomes among white, rural women independent of psychosocial and demographic correlates. J Hum Lact, 2004, 20(1): 18-29.
43.	Rasmussen KM, Kjolhede CL. Prepregnant overweight and obesity diminish the prolactin response to suckling in the first week postpartum. Pediatrics, 2004, 113(5): e465-471.
44.	Donath SM, Amir LH. Does maternal obesity adversely affect breastfeeding initiation and duration. J Paediatr Child Health, 2000, 36(5): 482-486.

1. 李玲. 妊娠期高血糖人群的类型和管理策略. 中华医学信息导报, 2021, 36(10): 12.
2. Silverman BL, Rizzo T, Green OC, et al. Long-term prospective evaluation of offspring of diabetic mothers. Diabetes, 1991, 40(Suppl 2): 121-125.
3. Buchanan TA, Xiang AH, Page KA. Gestational diabetes mellitus: risks and management during and after pregnancy. Nat Rev Endocrinol, 2012, 8(11): 639-649.
4. Woo JG, Martin LJ. Does breastfeeding protect against childhood obesity. Moving beyond observational evidence. Curr Obes Rep, 2015, 4(2): 207-216.
5. Cope MB, Allison DB. Critical review of the World Health Organization's (WHO) 2007 report on 'evidence of the long-term effects of breastfeeding: systematic reviews and meta-analysis' with respect to obesity. Obes Rev, 2008, 9(6): 594-605.
6. Weng SF, Redsell SA, Swift JA, et al. Systematic review and meta-analyses of risk factors for childhood overweight identifiable during infancy. Arch Dis Child, 2012, 97(12): 1019-1026.
7. Fenger-Grøn J, Fenger-Grøn M, Blunck CH, et al. Low breastfeeding rates and body mass index in Danish children of women with gestational diabetes mellitus. Int Breastfeed J, 2015, 10: 26.
8. Hui LL, Li AM, Nelson EAS, et al. In utero exposure to gestational diabetes and adiposity: does breastfeeding make a difference. Int J Obes (Lond), 2018, 42(7): 1317-1325.
9. Matias SL, Dewey KG, Quesenberry CP, et al. Maternal prepregnancy obesity and insulin treatment during pregnancy are independently associated with delayed lactogenesis in women with recent gestational diabetes mellitus. Am J Clin Nutr, 2014, 99(1): 115-121.
10. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
11. Higgins JPT, Thomas J, Chandler J, et al. Cochrane handbook for systematic reviews of interventions. 2nd Edition. Chichester (UK): John Wiley & Sons, 2019.
12. 赵亚玲, 马润玫, 黄永坤, 等. 母乳喂养对妊娠期糖尿病母亲子代儿童期超重的影响. 中国当代儿科杂志, 2013, 15(1): 56-61.
13. Schaefer-Graf UM, Hartmann R, Pawliczak J, et al. Association of breast-feeding and early childhood overweight in children from mothers with gestational diabetes mellitus. Diabetes Care, 2006, 29(5): 1105-1107.
14. Huvinen E, Tuomaala AK, Bergman PH, et al. Ascending growth is associated with offspring adiposity in pregnancies complicated with obesity or gestational diabetes. J Clin Endocrinol Metab, 2021, 106(5): e1993-e2004.
15. Mayer-Davis EJ, Rifas-Shiman SL, Zhou L, et al. Breast-feeding and risk for childhood obesity: does maternal diabetes or obesity status matter. Diabetes Care, 2006, 29(10): 2231-2237.
16. Vandyousefi S, Whaley SE, Widen EM, et al. Association of breastfeeding and early exposure to sugar-sweetened beverages with obesity prevalence in offspring born to mothers with and without gestational diabetes mellitus. Pediatr Obes, 2019, 14(12): e12569.
17. Faith MS, Hittner JB, Hurston SR, et al. Association of infant temperament with subsequent obesity in young children of mothers with gestational diabetes mellitus. JAMA Pediatr, 2019, 173(5): 424-433.
18. Plagemann A, Harder T, Franke K, et al. Long-term impact of neonatal breast-feeding on body weight and glucose tolerance in children of diabetic mothers. Diabetes Care, 2002, 25(1): 16-22.
19. Rodekamp E, Harder T, Kohlhoff R, et al. Long-term impact of breast-feeding on body weight and glucose tolerance in children of diabetic mothers: role of the late neonatal period and early infancy. Diabetes Care, 2005, 28(6): 1457-1462.
20. Zhao YL, Ma RM, Lao TT, et al. Maternal gestational diabetes mellitus and overweight and obesity in offspring: a study in Chinese children. J Dev Orig Health Dis, 2015, 6(6): 479-484.
21. Kaul P, Bowker SL, Savu A, et al. Association between maternal diabetes, being large for gestational age and breast-feeding on being overweight or obese in childhood. Diabetologia, 2019, 62(2): 249-258.
22. Hummel S, Weiß A, Bonifacio E, et al. Associations of breastfeeding with childhood autoimmunity, allergies, and overweight: The Environmental Determinants of Diabetes in the Young (TEDDY) study. Am J Clin Nutr, 2021, 114(1): 134-142.
23. Hummel S, Pflüger M, Kreichauf S, et al. Predictors of overweight during childhood in offspring of parents with type 1 diabetes. Diabetes Care, 2009, 32(5): 921-925.
24. Feig DS, Lipscombe LL, Tomlinson G, et al. Breastfeeding predicts the risk of childhood obesity in a multi-ethnic cohort of women with diabetes. J Matern Fetal Neonatal Med, 2011, 24(3): 511-515.
25. Birch LL, Fisher JO. Development of eating behaviors among children and adolescents. Pediatrics. 1998, 101(3 Pt 2): 539-549.
26. Lucas A, Boyes S, Bloom SR, et al. Metabolic and endocrine responses to a milk feed in six-day-old term infants: differences between breast and cow's milk formula feeding. Acta Paediatr Scand, 1981, 70(2): 195-200.
27. Lucas A, Sarson DL, Blackburn AM, et al. Breast vs bottle: endocrine responses are different with formula feeding. Lancet, 1980, 1(8181): 1267-1269.
28. Weber M, Grote V, Closa-Monasterolo R, et al. Lower protein content in infant formula reduces BMI and obesity risk at school age: follow-up of a randomized trial. Am J Clin Nutr, 2014, 99(5): 1041-1051.
29. Assunção ML, Ferreira HS, Coutinho SB, et al. Protective effect of breastfeeding against overweight can be detected as early as the second year of life: a study of children from one of the most socially-deprived areas of Brazil. J Health Popul Nutr, 2015, 33(1): 85-91.
30. Zheng JS, Liu H, Li J, et al. Exclusive breastfeeding is inversely associated with risk of childhood overweight in a large Chinese cohort. J Nutr, 2014, 144(9): 1454-1459.
31. 叶慧. 妊娠期糖尿病对产后不同泌乳阶段母乳营养成分及微生物多样性影响研究. 福州: 福建医科大学, 2021.
32. Qiao J, Dai LJ, Zhang Q, et al. A meta-analysis of the association between breastfeeding and early childhood obesity. J Pediatr Nurs, 2020, 53: 57-66.
33. 许金婷. 妊娠期糖尿病对婴幼儿肥胖的影响. 济南: 山东大学, 2018.
34. Gillman MW, Rifas-Shiman SL, Camargo CA, et al. Risk of overweight among adolescents who were breastfed as infants. JAMA, 2001, 285(19): 2461-2467.
35. Harder T, Bergmann R, Kallischnigg G, et al. Duration of breastfeeding and risk of overweight: a meta-analysis. Am J Epidemiol, 2005, 162(5): 397-403.
36. Dror DK, Allen LH. Retinol-to-fat ratio and retinol concentration in human milk show similar time trends and associations with maternal factors at the population level: a systematic review and meta-analysis. Adv Nutr, 2018, 9(suppl_1): 332S-346S.
37. Stettler N, Stallings VA, Troxel AB, et al. Weight gain in the first week of life and overweight in adulthood: a cohort study of European American subjects fed infant formula. Circulation, 2005, 111(15): 1897-1903.
38. Anderson SE, Keim SA. Parent-child interaction, self-regulation, and obesity prevention in early childhood. Curr Obes Rep, 2016, 5(2): 192-200.
39. 齐芮宁, 李立梅, 陈静. 国内外妊娠期糖尿病产妇母乳喂养影响因素及促进措施的研究进展. 中华现代护理杂志, 2019, 25(20): 2632-2636.
40. 张绍敏. 产后不同阶段妊娠糖尿病产妇母乳喂养状况及影响因素研究. 中国妇幼保健, 2015, 30(33): 5765-5767.
41. Jagiello KP, Azulay Chertok IR. Women's experiences with early breastfeeding after gestational diabetes. J Obstet Gynecol Neonatal Nurs, 2015, 44(4): 500-509.
42. Hilson JA, Rasmussen KM, Kjolhede CL. High prepregnant body mass index is associated with poor lactation outcomes among white, rural women independent of psychosocial and demographic correlates. J Hum Lact, 2004, 20(1): 18-29.
43. Rasmussen KM, Kjolhede CL. Prepregnant overweight and obesity diminish the prolactin response to suckling in the first week postpartum. Pediatrics, 2004, 113(5): e465-471.
44. Donath SM, Amir LH. Does maternal obesity adversely affect breastfeeding initiation and duration. J Paediatr Child Health, 2000, 36(5): 482-486.

Chinese Journal of Evidence-Based Medicine

Effects of breastfeeding on reducing the risk of overweight and obesity among offspring exposed to intrauterine hyperglycemia: a meta-analysis

Abstract Full text Figures/Tables Video References Cited by

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