Top

Published in:

01-12-2021 | Gestational Diabetes | Research article

Intensive lactation among women with recent gestational diabetes significantly alters the early postpartum circulating lipid profile: the SWIFT study

Authors: Ziyi Zhang, Mi Lai, Anthony L. Piro, Stacey E. Alexeeff, Amina Allalou, Hannes L. Röst, Feihan F. Dai, Michael B. Wheeler, Erica P. Gunderson

Published in: BMC Medicine | Issue 1/2021

Abstract

Background

Women with a history of gestational diabetes mellitus (GDM) have a 7-fold higher risk of developing type 2 diabetes (T2D). It is estimated that 20-50% of women with GDM history will progress to T2D within 10 years after delivery. Intensive lactation could be negatively associated with this risk, but the mechanisms behind a protective effect remain unknown.

Methods

In this study, we utilized a prospective GDM cohort of 1010 women without T2D at 6-9 weeks postpartum (study baseline) and tested for T2D onset up to 8 years post-baseline (n=980). Targeted metabolic profiling was performed on fasting plasma samples collected at both baseline and follow-up (1-2 years post-baseline) during research exams in a subset of 350 women (216 intensive breastfeeding, IBF vs. 134 intensive formula feeding or mixed feeding, IFF/Mixed). The relationship between lactation intensity and circulating metabolites at both baseline and follow-up were evaluated to discover underlying metabolic responses of lactation and to explore the link between these metabolites and T2D risk.

Results

We observed that lactation intensity was strongly associated with decreased glycerolipids (TAGs/DAGs) and increased phospholipids/sphingolipids at baseline. This lipid profile suggested decreased lipogenesis caused by a shift away from the glycerolipid metabolism pathway towards the phospholipid/sphingolipid metabolism pathway as a component of the mechanism underlying the benefits of lactation. Longitudinal analysis demonstrated that this favorable lipid profile was transient and diminished at 1-2 years postpartum, coinciding with the cessation of lactation. Importantly, when stratifying these 350 women by future T2D status during the follow-up (171 future T2D vs. 179 no T2D), we discovered that lactation induced robust lipid changes only in women who did not develop incident T2D. Subsequently, we identified a cluster of metabolites that strongly associated with future T2D risk from which we developed a predictive metabolic signature with a discriminating power (AUC) of 0.78, superior to common clinical variables (i.e., fasting glucose, AUC 0.56 or 2-h glucose, AUC 0.62).

Conclusions

In this study, we show that intensive lactation significantly alters the circulating lipid profile at early postpartum and that women who do not respond metabolically to lactation are more likely to develop T2D. We also discovered a 10-analyte metabolic signature capable of predicting future onset of T2D in IBF women. Our findings provide novel insight into how lactation affects maternal metabolism and its link to future diabetes onset.

Trial registration

ClinicalTrials.gov NCT01967030.

Available only for authorised users

Sobti J, Mathur GP, Gupta A, Who. WHO’s proposed global strategy for infant and young child feeding: a viewpoint. J Indian Med Assoc. 2002;100(8):502–4 506.PubMed

Victora CG, Rollins NC, Murch S, Krasevec J, Bahl R. Breastfeeding in the 21st century - Authors' reply. Lancet. 2016;387(10033):2089–90. https://doi.org/10.1016/S0140-6736(16)30538-4.CrossRefPubMed

Matias SL, Dewey KG, Quesenberry CP Jr, Gunderson EP. 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):115–21. https://doi.org/10.3945/ajcn.113.073049.CrossRefPubMed

Gunderson EP, Jacobs DR Jr, Chiang V, Lewis CE, Feng J, Quesenberry CP Jr, et al. Duration of lactation and incidence of the metabolic syndrome in women of reproductive age according to gestational diabetes mellitus status: a 20-Year prospective study in CARDIA (Coronary Artery Risk Development in Young Adults). Diabetes. 2010;59(2):495–504. https://doi.org/10.2337/db09-1197.CrossRefPubMed

Cohen A, Pieper CF, Brown AJ, Bastian LA. Number of children and risk of metabolic syndrome in women. J Women's Health (Larchmt). 2006;15(6):763–73. https://doi.org/10.1089/jwh.2006.15.763.CrossRef

Schwarz EB, Ray RM, Stuebe AM, Allison MA, Ness RB, Freiberg MS, et al. Duration of lactation and risk factors for maternal cardiovascular disease. Obstet Gynecol. 2009;113(5):974–82. https://doi.org/10.1097/01.AOG.0000346884.67796.ca.CrossRefPubMedPubMedCentral

Gunderson EP, Lewis CE, Lin Y, Sorel M, Gross M, Sidney S, et al. Lactation duration and progression to diabetes in women across the childbearing years: the 30-year CARDIA study. JAMA Intern Med. 2018;178(3):328–37. https://doi.org/10.1001/jamainternmed.2017.7978.CrossRefPubMedPubMedCentral

Gunderson EP, Hurston SR, Ning X, Lo JC, Crites Y, Walton D, et al. Lactation and progression to type 2 diabetes mellitus after gestational diabetes mellitus: a prospective cohort study. Ann Intern Med. 2015;163(12):889–98. https://doi.org/10.7326/M15-0807.CrossRefPubMedPubMedCentral

Ajmera VH, Terrault NA, VanWagner LB, Sarkar M, Lewis CE, Carr JJ, et al. Longer lactation duration is associated with decreased prevalence of non-alcoholic fatty liver disease in women. J Hepatol. 2019;70(1):126–32. https://doi.org/10.1016/j.jhep.2018.09.013.CrossRefPubMed

10.

Rameez RM, Sadana D, Kaur S, Ahmed T, Patel J, Khan MS, et al. Association of maternal lactation with diabetes and hypertension: a systematic review and meta-analysis. JAMA Netw Open. 2019;2(10):e1913401. https://doi.org/10.1001/jamanetworkopen.2019.13401.CrossRefPubMedPubMedCentral

11.

Stuebe AM, Rich-Edwards JW, Willett WC, Manson JE, Michels KB. Duration of lactation and incidence of type 2 diabetes. JAMA. 2005;294(20):2601–10. https://doi.org/10.1001/jama.294.20.2601.CrossRefPubMed

12.

Villegas R, Gao YT, Yang G, Li HL, Elasy T, Zheng W, et al. Duration of breast-feeding and the incidence of type 2 diabetes mellitus in the Shanghai Women’s Health Study. Diabetologia. 2008;51(2):258–66. https://doi.org/10.1007/s00125-007-0885-8.CrossRefPubMed

13.

Jager S, Jacobs S, Kroger J, Fritsche A, Schienkiewitz A, Rubin D, et al. Breast-feeding and maternal risk of type 2 diabetes: a prospective study and meta-analysis. Diabetologia. 2014;57(7):1355–65. https://doi.org/10.1007/s00125-014-3247-3.CrossRefPubMedPubMedCentral

14.

The global challenge of diabetes. Lancet. 2008;371(9626):1723.

15.

Zhu Y, Zhang C. Prevalence of gestational diabetes and risk of progression to type 2 diabetes: a global perspective. Curr Diab Rep. 2016;16(1):7. https://doi.org/10.1007/s11892-015-0699-x.CrossRefPubMedPubMedCentral

16.

Hunt KJ, Schuller KL. The increasing prevalence of diabetes in pregnancy. Obstet Gynecol Clin N Am. 2007;34(2):173–99, vii. https://doi.org/10.1016/j.ogc.2007.03.002.CrossRef

17.

Bellamy L, Casas JP, Hingorani AD, Williams D. Type 2 diabetes mellitus after gestational diabetes: a systematic review and meta-analysis. Lancet. 2009;373(9677):1773–9. https://doi.org/10.1016/S0140-6736(09)60731-5.CrossRefPubMed

18.

Puhkala J, Raitanen J, Kolu P, Tuominen P, Husu P, Luoto R. Metabolic syndrome in Finnish women 7 years after a gestational diabetes prevention trial. BMJ Open. 2017;7(3):e014565. https://doi.org/10.1136/bmjopen-2016-014565.CrossRefPubMedPubMedCentral

19.

Rhee EP, Cheng S, Larson MG, Walford GA, Lewis GD, McCabe E, et al. Lipid profiling identifies a triacylglycerol signature of insulin resistance and improves diabetes prediction in humans. J Clin Invest. 2011;121(4):1402–11. https://doi.org/10.1172/JCI44442.CrossRefPubMedPubMedCentral

20.

Razquin C, Toledo E, Clish CB, Ruiz-Canela M, Dennis C, Corella D, et al. Plasma lipidomic profiling and risk of type 2 diabetes in the PREDIMED Trial. Diabetes Care. 2018;41(12):2617–24. https://doi.org/10.2337/dc18-0840.CrossRefPubMedPubMedCentral

21.

Kjos SL, Henry O, Lee RM, Buchanan TA, Mishell DR Jr. The effect of lactation on glucose and lipid metabolism in women with recent gestational diabetes. Obstet Gynecol. 1993;82(3):451–5.PubMed

22.

Gunderson EP, Kim C, Quesenberry CP Jr, Marcovina S, Walton D, Azevedo RA, et al. Lactation intensity and fasting plasma lipids, lipoproteins, non-esterified free fatty acids, leptin and adiponectin in postpartum women with recent gestational diabetes mellitus: the SWIFT cohort. Metabolism. 2014;63(7):941–50. https://doi.org/10.1016/j.metabol.2014.04.006.CrossRefPubMedPubMedCentral

23.

Gunderson EP, Lewis CE, Wei GS, Whitmer RA, Quesenberry CP, Sidney S. Lactation and changes in maternal metabolic risk factors. Obstet Gynecol. 2007;109(3):729–38. https://doi.org/10.1097/01.AOG.0000252831.06695.03.CrossRefPubMedPubMedCentral

24.

Much D, Beyerlein A, Kindt A, Krumsiek J, Stuckler F, Rossbauer M, et al. Lactation is associated with altered metabolomic signatures in women with gestational diabetes. Diabetologia. 2016;59(10):2193–202. https://doi.org/10.1007/s00125-016-4055-8.CrossRefPubMed

25.

American Diabetes A. 12. Management of diabetes in pregnancy. Diabetes Care. 2016;39(Suppl 1):S94–8.

26.

Allalou A, Nalla A, Prentice KJ, Liu Y, Zhang M, Dai FF, et al. A predictive metabolic signature for the transition from gestational diabetes mellitus to type 2 diabetes. Diabetes. 2016;65(9):2529–39. https://doi.org/10.2337/db15-1720.CrossRefPubMedPubMedCentral

27.

Abdul-Ghani MA, Lyssenko V, Tuomi T, DeFronzo RA, Groop L. Fasting versus postload plasma glucose concentration and the risk for future type 2 diabetes: results from the Botnia Study. Diabetes Care. 2009;32(2):281–6. https://doi.org/10.2337/dc08-1264.CrossRefPubMedPubMedCentral

28.

Janghorbani M, Almasi SZ, Amini M. The product of triglycerides and glucose in comparison with fasting plasma glucose did not improve diabetes prediction. Acta Diabetol. 2015;52(4):781–8. https://doi.org/10.1007/s00592-014-0709-5.CrossRefPubMed

29.

Liu J, Semiz S, van der Lee SJ, van der Spek A, Verhoeven A, van Klinken JB, et al. Metabolomics based markers predict type 2 diabetes in a 14-year follow-up study. Metabolomics. 2017;13(9):104. https://doi.org/10.1007/s11306-017-1239-2.CrossRefPubMedPubMedCentral

30.

Carpenter MW, Coustan DR. Criteria for screening tests for gestational diabetes. Am J Obstet Gynecol. 1982;144(7):768–73. https://doi.org/10.1016/0002-9378(82)90349-0.CrossRefPubMed

31.

Gunderson EP, Matias SL, Hurston SR, Dewey KG, Ferrara A, Quesenberry CP Jr, 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(1):952. https://doi.org/10.1186/1471-2458-11-952.CrossRefPubMedPubMedCentral

32.

Expert Committee on the D, Classification of Diabetes M. Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care. 2003;26(Suppl 1):S5–20.

33.

Vandyousefi S, Davis JN, Gunderson EP. Association of infant diet with subsequent obesity at 2-5 years among children exposed to gestational diabetes: the SWIFT study. Diabetologia. 2021;64(5):1121–32. https://doi.org/10.1007/s00125-020-05379-y.CrossRefPubMed

34.

Piper S, Parks PL. Use of an intensity ratio to describe breastfeeding exclusivity in a national sample. J Hum Lact. 2001;17(3):227–32. https://doi.org/10.1177/089033440101700306.CrossRefPubMed

35.

Chong J, Soufan O, Li C, Caraus I, Li S, Bourque G, et al. MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res. 2018;46(W1):W486–94. https://doi.org/10.1093/nar/gky310.CrossRefPubMedPubMedCentral

36.

Lai M, Al Rijjal D, Rost HL, Dai FF, Gunderson EP, Wheeler MB. Underlying dyslipidemia postpartum in women with a recent GDM pregnancy who develop type 2 diabetes. Elife. 2020;9. https://doi.org/10.7554/eLife.59153.

37.

Reilly M, Torrang A, Klint A. Re-use of case-control data for analysis of new outcome variables. Stat Med. 2005;24(24):4009–19. https://doi.org/10.1002/sim.2398.CrossRefPubMed

38.

Jiang Y, Scott AJ, Wild CJ. Secondary analysis of case-control data. Stat Med. 2006;25(8):1323–39. https://doi.org/10.1002/sim.2283.CrossRefPubMed

39.

Hinshaw SJ, Lee AHY, Gill EE, Hancock REW. MetaBridge: enabling network-based integrative analysis via direct protein interactors of metabolites. Bioinformatics. 2018;34(18):3225–7. https://doi.org/10.1093/bioinformatics/bty331.CrossRefPubMed

40.

Janky R, Verfaillie A, Imrichova H, Van de Sande B, Standaert L, Christiaens V, et al. iRegulon: from a gene list to a gene regulatory network using large motif and track collections. PLoS Comput Biol. 2014;10(7):e1003731. https://doi.org/10.1371/journal.pcbi.1003731.CrossRefPubMedPubMedCentral

41.

Kennedy EP, Weiss SB. The function of cytidine coenzymes in the biosynthesis of phospholipides. J Biol Chem. 1956;222(1):193–214. https://doi.org/10.1016/S0021-9258(19)50785-2.CrossRefPubMed

42.

Mullen TD, Hannun YA, Obeid LM. Ceramide synthases at the centre of sphingolipid metabolism and biology. Biochem J. 2012;441(3):789–802. https://doi.org/10.1042/BJ20111626.CrossRefPubMed

43.

Nakahara K, Ohkuni A, Kitamura T, Abe K, Naganuma T, Ohno Y, et al. The Sjogren-Larsson syndrome gene encodes a hexadecenal dehydrogenase of the sphingosine 1-phosphate degradation pathway. Mol Cell. 2012;46(4):461–71. https://doi.org/10.1016/j.molcel.2012.04.033.CrossRefPubMed

44.

Jakobsson A, Westerberg R, Jacobsson A. Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog Lipid Res. 2006;45(3):237–49. https://doi.org/10.1016/j.plipres.2006.01.004.CrossRefPubMed

45.

Hutton JC, O'Brien RM. Glucose-6-phosphatase catalytic subunit gene family. J Biol Chem. 2009;284(43):29241–5. https://doi.org/10.1074/jbc.R109.025544.CrossRefPubMedPubMedCentral

46.

Henneberry AL, McMaster CR. Cloning and expression of a human choline/ethanolaminephosphotransferase: synthesis of phosphatidylcholine and phosphatidylethanolamine. Biochem J. 1999;339(Pt 2):291–8. https://doi.org/10.1042/bj3390291.CrossRefPubMedPubMedCentral

47.

Kallio MJ, Siimes MA, Perheentupa J, Salmenpera L, Miettinen TA. Serum cholesterol and lipoprotein concentrations in mothers during and after prolonged exclusive lactation. Metabolism. 1992;41(12):1327–30. https://doi.org/10.1016/0026-0495(92)90103-h.CrossRefPubMed

48.

van Stiphout WA, Hofman A, de Bruijn AM. Serum lipids in young women before, during, and after pregnancy. Am J Epidemiol. 1987;126(5):922–8. https://doi.org/10.1093/oxfordjournals.aje.a114729.CrossRefPubMed

49.

Piechota W, Staszewski A. Reference ranges of lipids and apolipoproteins in pregnancy. Eur J Obstet Gynecol Reprod Biol. 1992;45(1):27–35. https://doi.org/10.1016/0028-2243(92)90190-A.CrossRefPubMed

50.

Ramos-Roman MA, Syed-Abdul MM, Adams-Huet B, Casey BM, Parks EJ. Lactation versus formula feeding: insulin, glucose, and fatty acid metabolism during the postpartum period. Diabetes. 2020;69(8):1624–35. https://doi.org/10.2337/db19-1226.CrossRefPubMedPubMedCentral

51.

Kaplan W, Sunehag AL, Dao H, Haymond MW. Short-term effects of recombinant human growth hormone and feeding on gluconeogenesis in humans. Metabolism. 2008;57(6):725–32. https://doi.org/10.1016/j.metabol.2008.01.009.CrossRefPubMedPubMedCentral

52.

Hodson L, Skeaff CM, Fielding BA. Fatty acid composition of adipose tissue and blood in humans and its use as a biomarker of dietary intake. Prog Lipid Res. 2008;47(5):348–80. https://doi.org/10.1016/j.plipres.2008.03.003.CrossRefPubMed

53.

Siler SQ, Neese RA, Hellerstein MK. De novo lipogenesis, lipid kinetics, and whole-body lipid balances in humans after acute alcohol consumption. Am J Clin Nutr. 1999;70(5):928–36. https://doi.org/10.1093/ajcn/70.5.928.CrossRefPubMed

54.

Hudgins LC, Seidman CE, Diakun J, Hirsch J. Human fatty acid synthesis is reduced after the substitution of dietary starch for sugar. Am J Clin Nutr. 1998;67(4):631–9. https://doi.org/10.1093/ajcn/67.4.631.CrossRefPubMed

55.

Hudgins LC, Hellerstein M, Seidman C, Neese R, Diakun J, Hirsch J. Human fatty acid synthesis is stimulated by a eucaloric low fat, high carbohydrate diet. J Clin Invest. 1996;97(9):2081–91. https://doi.org/10.1172/JCI118645.CrossRefPubMedPubMedCentral

56.

King IB, Lemaitre RN, Kestin M. Effect of a low-fat diet on fatty acid composition in red cells, plasma phospholipids, and cholesterol esters: investigation of a biomarker of total fat intake. Am J Clin Nutr. 2006;83(2):227–36. https://doi.org/10.1093/ajcn/83.2.227.CrossRefPubMed

57.

McManaman JL. Formation of milk lipids: a molecular perspective. Clin Lipidol. 2009;4(3):391–401. https://doi.org/10.2217/clp.09.15.CrossRefPubMedPubMedCentral

58.

Kersten S. Integrated physiology and systems biology of PPARalpha. Mol Metab. 2014;3(4):354–71. https://doi.org/10.1016/j.molmet.2014.02.002.CrossRefPubMedPubMedCentral

59.

Shimano H, Yahagi N, Amemiya-Kudo M, Hasty AH, Osuga J, Tamura Y, et al. Sterol regulatory element-binding protein-1 as a key transcription factor for nutritional induction of lipogenic enzyme genes. J Biol Chem. 1999;274(50):35832–9. https://doi.org/10.1074/jbc.274.50.35832.CrossRefPubMed

60.

van Gastel N, Stegen S, Eelen G, Schoors S, Carlier A, Daniels VW, et al. Lipid availability determines fate of skeletal progenitor cells via SOX9. Nature. 2020;579(7797):111–7. https://doi.org/10.1038/s41586-020-2050-1.CrossRefPubMedPubMedCentral

61.

Oliver CH, Watson CJ. Making milk: a new link between STAT5 and Akt1. JAKSTAT. 2013;2(2):e23228. https://doi.org/10.4161/jkst.23228.CrossRefPubMedPubMedCentral

62.

Knopp RH, Walden CE, Wahl PW, Bergelin R, Chapman M, Irvine S, et al. Effect of postpartum lactation on lipoprotein lipids and apoproteins. J Clin Endocrinol Metab. 1985;60(3):542–7. https://doi.org/10.1210/jcem-60-3-542.CrossRefPubMed

63.

Sun HZ, Shi K, Wu XH, Xue MY, Wei ZH, Liu JX, et al. Lactation-related metabolic mechanism investigated based on mammary gland metabolomics and 4 biofluids’ metabolomics relationships in dairy cows. BMC Genomics. 2017;18(1):936. https://doi.org/10.1186/s12864-017-4314-1.CrossRefPubMedPubMedCentral

64.

Berg JM, Tymoczko J, Stryer L.: Section 26.1, phosphatidate is a common intermediate in the synthesis of phospholipids and triacylglycerols.; 2002.

65.

Funai K, Lodhi IJ, Spears LD, Yin L, Song H, Klein S, et al. Skeletal muscle phospholipid metabolism regulates insulin sensitivity and contractile function. Diabetes. 2016;65(2):358–70. https://doi.org/10.2337/db15-0659.CrossRefPubMed

66.

Hanamatsu H, Ohnishi S, Sakai S, Yuyama K, Mitsutake S, Takeda H, et al. Altered levels of serum sphingomyelin and ceramide containing distinct acyl chains in young obese adults. Nutr Diabetes. 2014;4(10):e141. https://doi.org/10.1038/nutd.2014.38.CrossRefPubMedPubMedCentral

67.

Sugimoto M, Shimizu Y, Zhao S, Ukon N, Nishijima K, Wakabayashi M, et al. Characterization of the role of sphingomyelin synthase 2 in glucose metabolism in whole-body and peripheral tissues in mice. Biochim Biophys Acta. 2016;1861(8 Pt A):688–702.CrossRef

68.

Selathurai A, Kowalski GM, Burch ML, Sepulveda P, Risis S, Lee-Young RS, et al. The CDP-ethanolamine pathway regulates skeletal muscle diacylglycerol content and mitochondrial biogenesis without altering insulin sensitivity. Cell Metab. 2015;21(5):718–30. https://doi.org/10.1016/j.cmet.2015.04.001.CrossRefPubMed

69.

Sokolowska E, Blachnio-Zabielska A. The role of ceramides in insulin resistance. Front Endocrinol. 2019;10:577. https://doi.org/10.3389/fendo.2019.00577.CrossRef

70.

Meikle PJ, Summers SA. Sphingolipids and phospholipids in insulin resistance and related metabolic disorders. Nat Rev Endocrinol. 2017;13(2):79–91. https://doi.org/10.1038/nrendo.2016.169.CrossRefPubMed

71.

Gunderson EP, Hedderson MM, Chiang V, Crites Y, Walton D, Azevedo RA, 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):50–6. https://doi.org/10.2337/dc11-1409.CrossRefPubMed

72.

Yasuhi I, Soda T, Yamashita H, Urakawa A, Izumi M, Kugishima Y, et al. The effect of high-intensity breastfeeding on postpartum glucose tolerance in women with recent gestational diabetes. Int Breastfeed J. 2017;12(1):32. https://doi.org/10.1186/s13006-017-0123-z.CrossRefPubMedPubMedCentral

73.

Baumgard LH, Collier RJ, Bauman DE. A 100-year review: regulation of nutrient partitioning to support lactation. J Dairy Sci. 2017;100(12):10353–66. https://doi.org/10.3168/jds.2017-13242.CrossRefPubMed

74.

Lenz S, Kuhl C, Hornnes PJ, Hagen C. Influence of lactation on oral glucose tolerance in the puerperium. Acta Endocrinol. 1981;98(3):428–31. https://doi.org/10.1530/acta.0.0980428.CrossRef

75.

Lai M, Liu Y, Ronnett GV, Wu A, Cox BJ, Dai FF, et al. Amino acid and lipid metabolism in post-gestational diabetes and progression to type 2 diabetes: a metabolic profiling study. PLoS Med. 2020;17(5):e1003112. https://doi.org/10.1371/journal.pmed.1003112.CrossRefPubMedPubMedCentral

76.

Li R, Jewell S, Grummer-Strawn L. Maternal obesity and breast-feeding practices. Am J Clin Nutr. 2003;77(4):931–6. https://doi.org/10.1093/ajcn/77.4.931.CrossRefPubMed

77.

Baker JL, Michaelsen KF, Sorensen TI, Rasmussen KM. High prepregnant body mass index is associated with early termination of full and any breastfeeding in Danish women. Am J Clin Nutr. 2007;86(2):404–11. https://doi.org/10.1093/ajcn/86.2.404.CrossRefPubMed

78.

Donath SM, Amir LH. Maternal obesity and initiation and duration of breastfeeding: data from the longitudinal study of Australian children. Matern Child Nutr. 2008;4(3):163–70. https://doi.org/10.1111/j.1740-8709.2008.00134.x.CrossRefPubMedPubMedCentral

79.

Winkvist A, Brantsaeter AL, Brandhagen M, Haugen M, Meltzer HM, Lissner L. Maternal prepregnant body mass index and gestational weight gain are associated with initiation and duration of breastfeeding among Norwegian mothers. J Nutr. 2015;145(6):1263–70. https://doi.org/10.3945/jn.114.202507.CrossRefPubMedPubMedCentral

80.

Nommsen-Rivers LA, Chantry CJ, Peerson JM, Cohen RJ, Dewey KG. Delayed onset of lactogenesis among first-time mothers is related to maternal obesity and factors associated with ineffective breastfeeding. Am J Clin Nutr. 2010;92(3):574–84. https://doi.org/10.3945/ajcn.2010.29192.CrossRefPubMed

81.

Wagner-Golbs A, Neuber S, Kamlage B, Christiansen N, Bethan B, Rennefahrt U, et al. Effects of long-term storage at -80 degrees C on the human plasma metabolome. Metabolites. 2019;9(5).

Title: Intensive lactation among women with recent gestational diabetes significantly alters the early postpartum circulating lipid profile: the SWIFT study
Authors: Ziyi Zhang
Mi Lai
Anthony L. Piro
Stacey E. Alexeeff
Amina Allalou
Hannes L. Röst
Feihan F. Dai
Michael B. Wheeler
Erica P. Gunderson
Publication date: 01-12-2021
Publisher: BioMed Central
Keywords: Gestational Diabetes
Lactation
Gestational Diabetes
Type 2 Diabetes
Published in: BMC Medicine / Issue 1/2021
Electronic ISSN: 1741-7015
DOI: https://doi.org/10.1186/s12916-021-02095-1

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Intensive lactation among women with recent gestational diabetes significantly alters the early postpartum circulating lipid profile: the SWIFT study

Abstract

Background

Methods

Results

Conclusions

Trial registration

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Trial registration

Please log in to get access to this content

Other articles of this Issue 1/2021

Sequelae, persistent symptomatology and outcomes after COVID-19 hospitalization: the ANCOHVID multicentre 6-month follow-up study

How robust are findings of pairwise and network meta-analysis in the presence of missing participant outcome data?

Glucocorticoids and breast cancer risk

Exposure assessment in early life: it is about time for multi-omics approaches

Parenteral artemisinins are associated with reduced mortality and neurologic deficits and improved long-term behavioral outcomes in children with severe malaria

Models based on nucleic acid methylation regulators will contribute to facilitating cancer precision medicine