The preventive effects of breastfeeding on progression to pre-diabetes mellitus (DM) and DM among females with prior gestational diabetes mellitus: a meta-analysis_Chinese Journal of Evidence-Based Medicine

Authors：

QIANG Wenjing ^1,2,3 , YU Xiayan ^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：

Gestational diabetes mellitus; Breastfeeding; Pre-diabetes mellitus; Diabetes mellitus; Meta-analysis; Systematic review; Cohort study

DOI：

10.7507/1672-2531.202105063

Video：

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Objective To systematically review the preventive effect of breastfeeding intensity and duration on progression to pre-diabetes mellitus (DM) and DM among females with prior gestational diabetes mellitus (GDM).Methods PubMed, Web of Science, CNKI, and WanFang Data databases were electronically searched to collect cohort studies on the correlation of GDM and breastfeeding from inception to January 8^th, 2021. Two reviewers independently screened literature, extracted data, and assessed the risk of bias of included studies. Meta-analysis was then performed using Stata 16.0 software.Results A total of 29 cohort studies were included. The results of the meta-analysis showed that breastfeeding could lower the risk of pre-DM (RR=0.64, 95%CI 0.57 to 0.71, P<0.001) and DM (RR=0.75, 95%CI 0.66 to 0.86, P<0.001) among females with prior GDM. Subgroup analysis showed that breastfeeding exhibited protective effects against pre-DM after 0 to 6 months as well as 6 to 12 months. Both breastfeeding for 0 to 6 months and over 12 months could decrease the risk of DM. These effects became prominent with the extension of the follow-up period. However, no significant association was observed between breastfeeding and recurrence of GDM (RR=0.72, 95%CI 0.47 to 1.09, P=0.14).Conclusions Breastfeeding may be a major contributor in protecting against pre-DM and DM among females with prior GDM history. Due to limited quality and quantity of the included studies, more high-quality studies are needed to verify the above conclusions.

Citation： QIANG Wenjing, YU Xiayan, ZHU Beibei, TAO Fangbiao. The preventive effects of breastfeeding on progression to pre-diabetes mellitus (DM) and DM among females with prior gestational diabetes mellitus: a meta-analysis. Chinese Journal of Evidence-Based Medicine, 2021, 21(9): 1082-1090. doi: 10.7507/1672-2531.202105063 Copy

1.	American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care, 2010, 33(Suppl 1): S62-S69.
2.	Bellamy L, Casas JP, Hingorani AD, et al. Type 2 diabetes mellitus after gestational diabetes: a systematic review and meta-analysis. Lancet, 2009, 373(9677): 1773-1779.
3.	Gunderson EP, Matias SL, Hurston SR, et al. Study of women, infant feeding, and type 2 diabetes mellitus after GDM pregnancy (SWIFT), a prospective cohort study: methodology and design. BMC Public Health, 2011, 11: 952.
4.	Metzger BE, Cho NH, Roston SM, et al. Prepregnancy weight and antepartum insulin secretion predict glucose tolerance five years after gestational diabetes mellitus. Diabetes Care, 1993, 16(12): 1598-1605.
5.	American Diabetes Association. 14. Management of diabetes in pregnancy: standards of medical care in diabetes-2021. Diabetes Care, 2021, 44(Suppl 1): S200-S210.
6.	Blumer I, Hadar E, Hadden DR, et al. Diabetes and pregnancy: an endocrine society clinical practice guideline. J Clin Endocrinol Metab, 2013, 98(11): 4227-4249.
7.	Thompson D, Berger H. Diabetes and pregnancy. Can J Diabetes, 2013, 37(Suppl 1): S168-S183.
8.	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.
9.	Ley SH, Chavarro JE, Li M, et al. Lactation duration and long-term risk for incident type 2 diabetes in women with a history of gestational diabetes mellitus. Diabetes Care, 2020, 43(4): 793-798.
10.	Zuarez-Easton S, Berkovich I, Birenbaum-Carmeli D, et al. Effect of lactation on the recurrence rate of gestational diabetes mellitus: a retrospective cohort study. Arch Gynecol Obstet, 2020, 301(4): 973-979.
11.	Reyes-López R, Perez-Luque E, Malacara JM. Relationship of lactation, BMI, and rs12255372 TCF7L2 polymorphism on the conversion to type 2 diabetes mellitus in women with previous gestational diabetes. Gynecol Endocrinol, 2019, 35(5): 412-416.
12.	张琰, 王晓彩, 孙晓. 母乳喂养对妊娠期糖尿病患者产后的影响. 中国现代医生, 2019, 57(7): 70-73.
13.	堵晓英, 陈道桢. 妊娠期糖尿病产妇产后恢复情况与新生儿喂养方式及个体化营养锻炼的相关性研究. 徐州医科大学学报, 2019, 39(8): 602-605.
14.	陈兵. 母乳喂养对妊娠糖尿病患者罹患 2 型糖尿病的保护效应观察. 糖尿病新世界, 2018, 21(17): 20-21.
15.	Shen Y, Leng J, Li W, et al. Lactation intensity and duration to postpartum diabetes and prediabetes risk in women with gestational diabetes. Diabetes Metab Res Rev, 2019, 35(3): e3115.
16.	游小红, 黄学明. 母乳喂养对妊娠糖尿病患者罹患 2 型糖尿病的保护性效应. 华中科技大学学报(医学版), 2018, 47(2): 236-239.
17.	Yasuhi I, Soda T, Yamashita H, et al. The effect of high-intensity breastfeeding on postpartum glucose tolerance in women with recent gestational diabetes. Int Breastfeed J, 2017, 12: 32.
18.	Corrado F, Giunta L, Granese R, et al. Metabolic effects of breastfeeding in women with previous gestational diabetes diagnosed according to the IADPSG criteria. J Matern Fetal Neonatal Med, 2019, 32(2): 225-228.
19.	赵春锋. 不同喂养方式对妊娠期糖尿病患者产后体质量指数和糖代谢恢复的影响. 中国妇幼保健, 2017, 32(23): 5989-5991.
20.	Martens PJ, Shafer LA, Dean HJ, et al. Breastfeeding initiation associated with reduced incidence of diabetes in mothers and offspring. Obstet Gynecol, 2016, 128(5): 1095-1104.
21.	Benhalima K, Jegers K, Devlieger R, et al. Glucose intolerance after a recent history of gestational diabetes based on the 2013 WHO criteria. PLoS One, 2016, 11(6): e0157272.
22.	范崇纯, 洪青, 朱卫红, 等. 不同喂养方式对妊娠期糖尿病患者产后恢复的影响. 解放军护理杂志, 2016, 33(3): 31-33, 51.
23.	Gunderson EP, Hurston SR, Ning X, et al. Lactation and progression to type 2 diabetes mellitus after gestational diabetes mellitus: a prospective cohort study. Ann Intern Med, 2015, 163(12): 889-898.
24.	Mattei L, Colatrella A, Bitterman O, et al. Long lasting effects of breastfeeding on metabolism in women with prior gestational diabetes. J Diabetes Mellitus, 2014, 4(4): 257-263.
25.	Capula C, Chiefari E, Vero A, et al. Prevalence and predictors of postpartum glucose intolerance in Italian women with gestational diabetes mellitus. Diabetes Res Clin Pract, 2014, 105(2): 223-230.
26.	Benhalima K, Leuridan L, Calewaert P, et al. Glucose intolerance after a recent history of gestational diabetes. Int J Endocrinol, 2014, 2014: 727652.
27.	Chouinard-Castonguay S, Weisnagel SJ, Tchernof A, et al. Relationship between lactation duration and insulin and glucose response among women with prior gestational diabetes. Eur J Endocrinol, 2013, 168(4): 515-523.
28.	Ziegler AG, Wallner M, Kaiser I, et al. Long-term protective effect of lactation on the development of type 2 diabetes in women with recent gestational diabetes mellitus. Diabetes, 2012, 61(12): 3167-3171.
29.	Kim SH, Kim MY, Yang JH, et al. Nutritional risk factors of early development of postpartum prediabetes and diabetes in women with gestational diabetes mellitus. Nutrition, 2011, 27(7-8): 782-788.
30.	Nelson AL, Le MH, Musherraf Z, et al. Intermediate-term glucose tolerance in women with a history of gestational diabetes: natural history and potential associations with breastfeeding and contraception. Am J Obstet Gynecol, 2008, 198(6): 699, e1-7.
31.	Stuebe AM, Rich-Edwards JW, Willett WC, et al. Duration of lactation and incidence of type 2 diabetes. JAMA, 2005, 294(20): 2601-2610.
32.	McManus RM, Cunningham I, Watson A, et al. Beta-cell function and visceral fat in lactating women with a history of gestational diabetes. Metabolism, 2001, 50(6): 715-719.
33.	MacNeill S, Dodds L, Hamilton DC, et al. Rates and risk factors for recurrence of gestational diabetes. Diabetes Care, 2001, 24(4): 659-662.
34.	Kjos SL, Peters RK, Xiang A, et al. Contraception and the risk of type 2 diabetes mellitus in Latina women with prior gestational diabetes mellitus. JAMA, 1998, 280(6): 533-538.
35.	Buchanan TA, Xiang A, Kjos SL, et al. Gestational diabetes: antepartum characteristics that predict postpartum glucose intolerance and type 2 diabetes in Latino women. Diabetes, 1998, 47(8): 1302-1310.
36.	Kjos SL, Henry O, Lee RM, et al. The effect of lactation on glucose and lipid metabolism in women with recent gestational diabetes. Obstet Gynecol, 1993, 82(3): 451-455.
37.	Oats JN, Beischer NA. The persistence of abnormal glucose tolerance after delivery. Obstet Gynecol, 1990, 75(3 Pt 1): 397-401.
38.	Gunderson EP, Hedderson MM, Chiang V, et al. Lactation intensity and postpartum maternal glucose tolerance and insulin resistance in women with recent GDM: the SWIFT cohort. Diabetes Care, 2012, 35(1): 50-56.
39.	Kramer MS, Kakuma R. The optimal duration of exclusive breastfeeding: a systematic review. Adv Exp Med Biol, 2004, 554: 63-77.
40.	Ramos-Román MA. Prolactin and lactation as modifiers of diabetes risk in gestational diabetes. Horm Metab Res, 2011, 43(9): 593-600.
41.	Duan Y, Yang Z, Lai J, et al. Exclusive breastfeeding rate and complementary feeding indicators in china: a national representative survey in 2013. Nutrients, 2018, 10(2): 249.
42.	Demirci JR, Bogen DL, Holland C, et al. Characteristics of breastfeeding discussions at the initial prenatal visit. Obstet Gynecol, 2013, 122(6): 1263-1270.
43.	Finkelstein SA, Keely E, Feig DS, et al. Breastfeeding in women with diabetes: lower rates despite greater rewards. A population-based study. Diabet Med, 2013, 30(9): 1094-1101.
44.	Kozhimannil KB, Jou J, Attanasio LB, et al. Medically complex pregnancies and early breastfeeding behaviors: a retrospective analysis. PLoS One, 2014, 9(8): e104820.
45.	Tanase-Nakao K, Arata N, Kawasaki M, et al. Potential protective effect of lactation against incidence of type 2 diabetes mellitus in women with previous gestational diabetes mellitus: a systematic review and meta-analysis. Diabetes Metab Res Rev, 2017, 33(4): e2875.

1. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care, 2010, 33(Suppl 1): S62-S69.
2. Bellamy L, Casas JP, Hingorani AD, et al. Type 2 diabetes mellitus after gestational diabetes: a systematic review and meta-analysis. Lancet, 2009, 373(9677): 1773-1779.
3. Gunderson EP, Matias SL, Hurston SR, et al. Study of women, infant feeding, and type 2 diabetes mellitus after GDM pregnancy (SWIFT), a prospective cohort study: methodology and design. BMC Public Health, 2011, 11: 952.
4. Metzger BE, Cho NH, Roston SM, et al. Prepregnancy weight and antepartum insulin secretion predict glucose tolerance five years after gestational diabetes mellitus. Diabetes Care, 1993, 16(12): 1598-1605.
5. American Diabetes Association. 14. Management of diabetes in pregnancy: standards of medical care in diabetes-2021. Diabetes Care, 2021, 44(Suppl 1): S200-S210.
6. Blumer I, Hadar E, Hadden DR, et al. Diabetes and pregnancy: an endocrine society clinical practice guideline. J Clin Endocrinol Metab, 2013, 98(11): 4227-4249.
7. Thompson D, Berger H. Diabetes and pregnancy. Can J Diabetes, 2013, 37(Suppl 1): S168-S183.
8. 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.
9. Ley SH, Chavarro JE, Li M, et al. Lactation duration and long-term risk for incident type 2 diabetes in women with a history of gestational diabetes mellitus. Diabetes Care, 2020, 43(4): 793-798.
10. Zuarez-Easton S, Berkovich I, Birenbaum-Carmeli D, et al. Effect of lactation on the recurrence rate of gestational diabetes mellitus: a retrospective cohort study. Arch Gynecol Obstet, 2020, 301(4): 973-979.
11. Reyes-López R, Perez-Luque E, Malacara JM. Relationship of lactation, BMI, and rs12255372 TCF7L2 polymorphism on the conversion to type 2 diabetes mellitus in women with previous gestational diabetes. Gynecol Endocrinol, 2019, 35(5): 412-416.
12. 张琰, 王晓彩, 孙晓. 母乳喂养对妊娠期糖尿病患者产后的影响. 中国现代医生, 2019, 57(7): 70-73.
13. 堵晓英, 陈道桢. 妊娠期糖尿病产妇产后恢复情况与新生儿喂养方式及个体化营养锻炼的相关性研究. 徐州医科大学学报, 2019, 39(8): 602-605.
14. 陈兵. 母乳喂养对妊娠糖尿病患者罹患 2 型糖尿病的保护效应观察. 糖尿病新世界, 2018, 21(17): 20-21.
15. Shen Y, Leng J, Li W, et al. Lactation intensity and duration to postpartum diabetes and prediabetes risk in women with gestational diabetes. Diabetes Metab Res Rev, 2019, 35(3): e3115.
16. 游小红, 黄学明. 母乳喂养对妊娠糖尿病患者罹患 2 型糖尿病的保护性效应. 华中科技大学学报(医学版), 2018, 47(2): 236-239.
17. Yasuhi I, Soda T, Yamashita H, et al. The effect of high-intensity breastfeeding on postpartum glucose tolerance in women with recent gestational diabetes. Int Breastfeed J, 2017, 12: 32.
18. Corrado F, Giunta L, Granese R, et al. Metabolic effects of breastfeeding in women with previous gestational diabetes diagnosed according to the IADPSG criteria. J Matern Fetal Neonatal Med, 2019, 32(2): 225-228.
19. 赵春锋. 不同喂养方式对妊娠期糖尿病患者产后体质量指数和糖代谢恢复的影响. 中国妇幼保健, 2017, 32(23): 5989-5991.
20. Martens PJ, Shafer LA, Dean HJ, et al. Breastfeeding initiation associated with reduced incidence of diabetes in mothers and offspring. Obstet Gynecol, 2016, 128(5): 1095-1104.
21. Benhalima K, Jegers K, Devlieger R, et al. Glucose intolerance after a recent history of gestational diabetes based on the 2013 WHO criteria. PLoS One, 2016, 11(6): e0157272.
22. 范崇纯, 洪青, 朱卫红, 等. 不同喂养方式对妊娠期糖尿病患者产后恢复的影响. 解放军护理杂志, 2016, 33(3): 31-33, 51.
23. Gunderson EP, Hurston SR, Ning X, et al. Lactation and progression to type 2 diabetes mellitus after gestational diabetes mellitus: a prospective cohort study. Ann Intern Med, 2015, 163(12): 889-898.
24. Mattei L, Colatrella A, Bitterman O, et al. Long lasting effects of breastfeeding on metabolism in women with prior gestational diabetes. J Diabetes Mellitus, 2014, 4(4): 257-263.
25. Capula C, Chiefari E, Vero A, et al. Prevalence and predictors of postpartum glucose intolerance in Italian women with gestational diabetes mellitus. Diabetes Res Clin Pract, 2014, 105(2): 223-230.
26. Benhalima K, Leuridan L, Calewaert P, et al. Glucose intolerance after a recent history of gestational diabetes. Int J Endocrinol, 2014, 2014: 727652.
27. Chouinard-Castonguay S, Weisnagel SJ, Tchernof A, et al. Relationship between lactation duration and insulin and glucose response among women with prior gestational diabetes. Eur J Endocrinol, 2013, 168(4): 515-523.
28. Ziegler AG, Wallner M, Kaiser I, et al. Long-term protective effect of lactation on the development of type 2 diabetes in women with recent gestational diabetes mellitus. Diabetes, 2012, 61(12): 3167-3171.
29. Kim SH, Kim MY, Yang JH, et al. Nutritional risk factors of early development of postpartum prediabetes and diabetes in women with gestational diabetes mellitus. Nutrition, 2011, 27(7-8): 782-788.
30. Nelson AL, Le MH, Musherraf Z, et al. Intermediate-term glucose tolerance in women with a history of gestational diabetes: natural history and potential associations with breastfeeding and contraception. Am J Obstet Gynecol, 2008, 198(6): 699, e1-7.
31. Stuebe AM, Rich-Edwards JW, Willett WC, et al. Duration of lactation and incidence of type 2 diabetes. JAMA, 2005, 294(20): 2601-2610.
32. McManus RM, Cunningham I, Watson A, et al. Beta-cell function and visceral fat in lactating women with a history of gestational diabetes. Metabolism, 2001, 50(6): 715-719.
33. MacNeill S, Dodds L, Hamilton DC, et al. Rates and risk factors for recurrence of gestational diabetes. Diabetes Care, 2001, 24(4): 659-662.
34. Kjos SL, Peters RK, Xiang A, et al. Contraception and the risk of type 2 diabetes mellitus in Latina women with prior gestational diabetes mellitus. JAMA, 1998, 280(6): 533-538.
35. Buchanan TA, Xiang A, Kjos SL, et al. Gestational diabetes: antepartum characteristics that predict postpartum glucose intolerance and type 2 diabetes in Latino women. Diabetes, 1998, 47(8): 1302-1310.
36. Kjos SL, Henry O, Lee RM, et al. The effect of lactation on glucose and lipid metabolism in women with recent gestational diabetes. Obstet Gynecol, 1993, 82(3): 451-455.
37. Oats JN, Beischer NA. The persistence of abnormal glucose tolerance after delivery. Obstet Gynecol, 1990, 75(3 Pt 1): 397-401.
38. Gunderson EP, Hedderson MM, Chiang V, et al. Lactation intensity and postpartum maternal glucose tolerance and insulin resistance in women with recent GDM: the SWIFT cohort. Diabetes Care, 2012, 35(1): 50-56.
39. Kramer MS, Kakuma R. The optimal duration of exclusive breastfeeding: a systematic review. Adv Exp Med Biol, 2004, 554: 63-77.
40. Ramos-Román MA. Prolactin and lactation as modifiers of diabetes risk in gestational diabetes. Horm Metab Res, 2011, 43(9): 593-600.
41. Duan Y, Yang Z, Lai J, et al. Exclusive breastfeeding rate and complementary feeding indicators in china: a national representative survey in 2013. Nutrients, 2018, 10(2): 249.
42. Demirci JR, Bogen DL, Holland C, et al. Characteristics of breastfeeding discussions at the initial prenatal visit. Obstet Gynecol, 2013, 122(6): 1263-1270.
43. Finkelstein SA, Keely E, Feig DS, et al. Breastfeeding in women with diabetes: lower rates despite greater rewards. A population-based study. Diabet Med, 2013, 30(9): 1094-1101.
44. Kozhimannil KB, Jou J, Attanasio LB, et al. Medically complex pregnancies and early breastfeeding behaviors: a retrospective analysis. PLoS One, 2014, 9(8): e104820.
45. Tanase-Nakao K, Arata N, Kawasaki M, et al. Potential protective effect of lactation against incidence of type 2 diabetes mellitus in women with previous gestational diabetes mellitus: a systematic review and meta-analysis. Diabetes Metab Res Rev, 2017, 33(4): e2875.

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The preventive effects of breastfeeding on progression to pre-diabetes mellitus (DM) and DM among females with prior gestational diabetes mellitus: a meta-analysis

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