Long-Term Effect of Lactation on Maternal Cardiovascular Function and Adiposity in a Murine Model

Sandra R. Herrera; Kathleen L. Vincent; Aaron Poole; Gayle Olson; Igor Patrikeev; Jamal Saada; Phyllis Gamble; Massoud Motamedi; George R. Saade; Alison M. Stuebe; Egle Bytautiene Prewit

doi:10.1055/s-0038-1669443

American Journal of Perinatology, Table of Contents

Am J Perinatol 2019; 36(05): 490-497
DOI: 10.1055/s-0038-1669443

Original Article

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Long-Term Effect of Lactation on Maternal Cardiovascular Function and Adiposity in a Murine Model

Sandra R. Herrera

¹Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, University of Texas Medical Branch, Galveston, Texas

,

Kathleen L. Vincent

²Division of Gynecology, Department of Obstetrics and Gynecology, Center for Biomedical Engineering, University of Texas Medical Branch, Galveston, Texas

,

Aaron Poole

¹Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, University of Texas Medical Branch, Galveston, Texas

,

Gayle Olson

¹Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, University of Texas Medical Branch, Galveston, Texas

,

Igor Patrikeev

³Center for Biomedical Engineering, University of Texas Medical Branch, Galveston, Texas

,

Jamal Saada

³Center for Biomedical Engineering, University of Texas Medical Branch, Galveston, Texas

,

Phyllis Gamble

¹Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, University of Texas Medical Branch, Galveston, Texas

,

Massoud Motamedi

³Center for Biomedical Engineering, University of Texas Medical Branch, Galveston, Texas

,

George R. Saade

¹Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, University of Texas Medical Branch, Galveston, Texas

,

Alison M. Stuebe

⁴Division of Maternal Fetal Medicine, Department of Obstetrics and Gynecology, University of North Carolina School of Medicine, Chapel Hill, North Carolina

⁵Department of Maternal and Child Health, University of North Carolina Gillings School of Public Health, Chapel Hill, North Carolina

,

Egle Bytautiene Prewit

¹Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, University of Texas Medical Branch, Galveston, Texas

› Author Affiliations

Abstract

Objective Epidemiological studies suggest that lactation is associated with long-term maternal health benefits. To avoid confounders in human studies, we used a previously characterized murine model to investigate the long-term effect of lactation on both cardiovascular function and adiposity.

Study Design After the delivery of the pups, CD-1 female mice were randomly divided into two groups: lactated and nonlactated (NL). Before pregnancy and at 9 months postdelivery, blood pressure was measured using a tail cuff, visceral adipose tissue (VAT) and subcutaneous adipose tissue (SAT) were assessed by computed tomography (CT), echocardiography was performed using microultrasound, and cholesterol panels and fasting blood glucose were measured. The data were analyzed using Student's t-test (significance at p < 0.05).

Results There were no differences in baseline parameters between the two groups. At 9 months postdelivery, the NL group weighed significantly more (p = 0.03) and demonstrated a significantly lower cardiac output (p = 0.05) and ejection fraction (p = 0.03). The mice in the NL group also had higher VAT (p < 0.01) and SAT percentiles (p = 0.03). Fasting glucose (p = 0.01) and low-density lipoprotein (p = 0.01) were significantly higher in the NL group at 9 months.

Conclusion Our results show the benefit of lactation is not just limited to the immediate postpartum period but it also extends into midlife in a murine model.

Keywords

adipose tissue - blood pressure - CD-1 mice - lactation - long-term effect

Full Text

References

References
1 Stuebe AM, Rich-Edwards JW, Willett WC, Manson JE, Michels KB. Duration of lactation and incidence of type 2 diabetes. JAMA 2005; 294 (20) 2601-2610
2 Schwarz EB, Ray RM, Stuebe AM. , et al. Duration of lactation and risk factors for maternal cardiovascular disease. Obstet Gynecol 2009; 113 (05) 974-982
3 Stuebe AM, Michels KB, Willett WC, Manson JE, Rexrode K, Rich-Edwards JW. Duration of lactation and incidence of myocardial infarction in middle to late adulthood. Am J Obstet Gynecol 2009; 200 (02) 138.e1-138.e8
4 Gunderson EP, Jacobs Jr DR, Chiang V. , 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 (02) 495-504
5 Ram KT, Bobby P, Hailpern SM. , et al. Duration of lactation is associated with lower prevalence of the metabolic syndrome in midlife--SWAN, the study of women's health across the nation. Am J Obstet Gynecol 2008; 198 (03) 268.e1-268.e6
6 Choi SR, Kim YM, Cho MS, Kim SH, Shim YS. Association between duration of breast feeding and metabolic syndrome: The Korean National Health and Nutrition Examination Surveys. J Womens Health (Larchmt) 2017; 26 (04) 361-367
7 Lee SY, Kim MT, Jee SH, Yang HP. Does long-term lactation protect premenopausal women against hypertension risk? A Korean women's cohort study. Prev Med 2005; 41 (02) 433-438
8 Klingberg S, Brekke HK, Winkvist A, Engström G, Hedblad B, Drake I. Parity, weight change, and maternal risk of cardiovascular events. Am J Obstet Gynecol 2017; 216 (02) 172.e1-172.e15
9 Countouris ME, Schwarz EB, Rossiter BC. , et al. Effects of lactation on postpartum blood pressure among women with gestational hypertension and preeclampsia. Am J Obstet Gynecol 2016; 215 (02) 241.e1-241.e8
10 Gunderson EP, Hurston SR, Ning X. , et al; Study of Women, Infant Feeding and Type 2 Diabetes After GDM Pregnancy Investigators. Lactation and progression to type 2 diabetes mellitus after gestational diabetes mellitus: a prospective cohort study. Ann Intern Med 2015; 163 (12) 889-898
11 Victora CG, Bahl R, Barros AJD. , et al; Lancet Breastfeeding Series Group. Breastfeeding in the 21st century: epidemiology, mechanisms, and lifelong effect. Lancet 2016; 387 (10017): 475-490
12 Stuebe AM. Does breastfeeding prevent the metabolic syndrome, or does the metabolic syndrome prevent breastfeeding?. Semin Perinatol 2015; 39 (04) 290-295
13 Beck LF, Morrow B, Lipscomb LE. , et al. Prevalence of selected maternal behaviors and experiences, Pregnancy Risk Assessment Monitoring System (PRAMS), 1999. MMWR Surveill Summ 2002; 51 (02) 1-27
14 Pesa JA, Shelton MM. Health-enhancing behaviors correlated with breastfeeding among a national sample of mothers. Public Health Nurs 1999; 16 (02) 120-124
15 Steingrimsdottir L, Brasel JA, Greenwood MRC. Diet, pregnancy, and lactation: effects on adipose tissue, lipoprotein lipase, and fat cell size. Metabolism 1980; 29 (09) 837-841
16 Moore BJ, Brasel JA. One cycle of reproduction consisting of pregnancy, lactation or no lactation, and recovery: effects on carcass composition in ad libitum-fed and food-restricted rats. J Nutr 1984; 114 (09) 1548-1559
17 Jones RG, Ilic V, Williamson DH. Physiological significance of altered insulin metabolism in the conscious rat during lactation. Biochem J 1984; 220 (02) 455-460
18 Poole AT, Vincent KL, Olson GL. , et al. Effect of lactation on maternal postpartum cardiac function and adiposity: a murine model. Am J Obstet Gynecol 2014; 211 (04) 424.e1-424.e7
19 Daugherty A, Rateri D, Hong L, Balakrishnan A. Measuring blood pressure in mice using volume pressure recording, a tail-cuff method. J Vis Exp 2009; (27) . pii: 1291
20 Feng M, Dipetrillo K. Non-invasive blood pressure measurement in mice. Methods Mol Biol 2009; 573: 45-55
21 Feng M, Whitesall S, Zhang Y, Beibel M, D'Alecy L, DiPetrillo K. Validation of volume-pressure recording tail-cuff blood pressure measurements. Am J Hypertens 2008; 21 (12) 1288-1291
22 Hildebrandt AL, Kelly-Sullivan DM, Black SC. Validation of a high-resolution X-ray computed tomography system to measure murine adipose tissue depot mass in situ and longitudinally. J Pharmacol Toxicol Methods 2002; 47 (02) 99-106
23 Luu YK, Lublinsky S, Ozcivici E. , et al. In vivo quantification of subcutaneous and visceral adiposity by micro-computed tomography in a small animal model. Med Eng Phys 2009; 31 (01) 34-41
24 Lublinsky S, Luu YK, Rubin CT, Judex S. Automated separation of visceral and subcutaneous adiposity in in vivo microcomputed tomographies of mice. J Digit Imaging 2009; 22 (03) 222-231
25 Judex S, Luu YK, Ozcivici E, Adler B, Lublinsky S, Rubin CT. Quantification of adiposity in small rodents using micro-CT. Methods 2010; 50 (01) 14-19
26 Stuebe AM, Rich-Edwards JW. The reset hypothesis: lactation and maternal metabolism. Am J Perinatol 2009; 26 (01) 81-88
27 Kinoshita T, Itoh M. Longitudinal variance of fat mass deposition during pregnancy evaluated by ultrasonography: the ratio of visceral fat to subcutaneous fat in the abdomen. Gynecol Obstet Invest 2006; 61 (02) 115-118
28 McClure CK, Catov J, Ness R, Schwarz EB. Maternal visceral adiposity by consistency of lactation. Matern Child Health J 2012; 16 (02) 316-321
29 McClure CK, Schwarz EB, Conroy MB, Tepper PG, Janssen I, Sutton-Tyrrell KC. Breastfeeding and subsequent maternal visceral adiposity. Obesity (Silver Spring) 2011; 19 (11) 2205-2213
30 Neeland IJ, Ayers CR, Rohatgi AK. , et al. Associations of visceral and abdominal subcutaneous adipose tissue with markers of cardiac and metabolic risk in obese adults. Obesity (Silver Spring) 2013; 21 (09) E439-E447
31 Akagiri S, Naito Y, Ichikawa H. , et al. A mouse model of metabolic syndrome; increase in visceral adipose tissue precedes the development of fatty liver and insulin resistance in high-fat diet-fed male KK/Ta mice. J Clin Biochem Nutr 2008; 42 (02) 150-157
32 Huffman DM, Barzilai N. Role of visceral adipose tissue in aging. Biochim Biophys Acta 2009; 1790 (10) 1117-1123
33 Schwarz EB, McClure CK, Tepper PG. , et al. Lactation and maternal measures of subclinical cardiovascular disease. Obstet Gynecol 2010; 115 (01) 41-48
34 Stuebe AM, Schwarz EB, Grewen K. , et al. Duration of lactation and incidence of maternal hypertension: a longitudinal cohort study. Am J Epidemiol 2011; 174 (10) 1147-1158
35 Villegas R, Gao YT, Yang G. , et al. Duration of breast-feeding and the incidence of type 2 diabetes mellitus in the Shanghai Women's Health Study. Diabetologia 2008; 51 (02) 258-266
36 Aune D, Norat T, Romundstad P, Vatten LJ. Breastfeeding and the maternal risk of type 2 diabetes: a systematic review and dose-response meta-analysis of cohort studies. Nutr Metab Cardiovasc Dis 2014; 24 (02) 107-115
37 Gunderson EP, Lewis CE, Wei GS, Whitmer RA, Quesenberry CP, Sidney S. Lactation and changes in maternal metabolic risk factors. Obstet Gynecol 2007; 109 (03) 729-738
38 Bartick MC, Stuebe AM, Schwarz EB, Luongo C, Reinhold AG, Foster EM. Cost analysis of maternal disease associated with suboptimal breastfeeding. Obstet Gynecol 2013; 122 (01) 111-119
39 Centers for Disease Control and Prevention. Breastfeeding among U.S. Children Born 2000–2009, CDC National Immunization Survey. 2012. Available at: https://www.cdc.gov/breastfeeding/data/nis_data/index.htm . Accessed April 7, 2013
40 Bai DL, Wu KM, Tarrant M. Association between intrapartum interventions and breastfeeding duration. J Midwifery Womens Health 2013; 58 (01) 25-32
41 French CA, Cong X, Chung KS. Labor epidural analgesia and breastfeeding: a systematic review. J Hum Lact 2016; 32 (03) 507-520
42 Hobbs AJ, Mannion CA, McDonald SW, Brockway M, Tough SC. The impact of caesarean section on breastfeeding initiation, duration and difficulties in the first four months postpartum. BMC Pregnancy Childbirth 2016; 16 (01) 90
43 Declercq ER, Sakala C, Corry MP, Applebaum S, Herrlich A. Major Survey Findings of Listening to Mothers(SM) III: New Mothers Speak Out: Report of National Surveys of Women's Childbearing Experiences Conducted October-December 2012 and January-April 2013. J Perinat Educ 2014; 23 (01) 17-24
44 Gu V, Feeley N, Gold I. , et al. Intrapartum synthetic oxytocin and its effects on maternal well-being at 2 months postpartum. Birth 2016; 43 (01) 28-35
45 Surtees PG, Wainwright NW, Luben RN, Wareham NJ, Bingham SA, Khaw KT. Depression and ischemic heart disease mortality: evidence from the EPIC-Norfolk United Kingdom prospective cohort study. Am J Psychiatry 2008; 165 (04) 515-523