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Nutrient and hormone composition of milk is altered in rodent dams post-bariatric surgery

Published online by Cambridge University Press:  09 August 2019

Evangeline M. Deer ,
Bradley Welch ,
Laura L. Hernandez ,
Randy J. Seeley  and
Bernadette E. Grayson Open the ORCID record for Bernadette E. Grayson [Opens in a new window]
Evangeline M. Deer
Affiliation:
Department of Neurobiology and Anatomical Sciences, University of Mississippi Medical Center, Jackson, MS, USA
Bradley Welch
Affiliation:
Department of Neurobiology and Anatomical Sciences, University of Mississippi Medical Center, Jackson, MS, USA
Laura L. Hernandez
Affiliation:
Department of Dairy Science, University of Wisconsin-Madison, Madison, WI, USA
Randy J. Seeley
Affiliation:
Department of Surgery, University of Michigan, Ann Arbor, MI, USA
Bernadette E. Grayson*
Affiliation:
Department of Neurobiology and Anatomical Sciences, University of Mississippi Medical Center, Jackson, MS, USA
*
Address for correspondence: Bernadette E. Grayson, Department of Neurobiology and Anatomical Sciences, University of Mississippi Medical Center, 2500 North State Street, Jackson, MS 39216, USA. Email: [email protected]; Phone: 601-984-6809; Fax: 601-984-1655
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Abstract

Although bariatric surgery is approved for a woman of child-bearing age with an interest in subsequent pregnancy, reports of in utero growth issues during pregnancy have garnered a closer look at the impact of maternal surgical weight loss on the pre- and postpartum periods. Offspring of dams having received vertical sleeve gastrectomy (VSG) are born small-for-gestational age and have increased risk for metabolic syndrome later in life. Here, we aimed to determine whether the postnatal catch-up growth trajectory of bariatric offspring may be affected by milk composition. Milk samples were collected at postnatal day 15/16 from dams having received VSG surgery and fed a high-fat diet (HFD) (H-VSG), Sham surgery and fed chow (C-Sham), or Sham surgery and fed HFD (H-Sham). Milk obtained from H-VSG dams had elevated glucose (P < 0.05) and significantly reduced triglyceride content (P < 0.01). Milk from H-Sham dams had the lowest amount of milk protein (P < 0.05). Fatty acid composition measured by fractionation was largely not affected by surgery but rather maternal diet. No difference was observed in milk leptin levels; however, insulin, adiponectin, and growth hormone levels were significantly increased in milk from H-VSG animals. H-Sham had the lowest level of immunoglobulin (Ig)A, whereas IgG was significantly reduced in H-VSG. Taken together, the quality of milk from H-VSG dams suggests that milk composition could be a factor in reducing the rate of growth during the lactation period.

Keywords

Bariatric surgerymilkobesityhormonesnutrients
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 11 , Issue 1 , February 2020 , pp. 71 - 77
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2019 

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References

Colquitt, JL, Pickett, K, Loveman, E, Frampton, GK. Surgery for weight loss in adults. Cochrane Database Syst Rev. 2014; 8, Cd003641. doi: 10.1002/14651858.CD003641.pub4.Google Scholar
Himpens, J, Dobbeleir, J, Peeters, G. Long-term results of laparoscopic sleeve gastrectomy for obesity. Ann Surg. 2010; 252, 319–324.CrossRefGoogle ScholarPubMed
Peterli, R, Wölnerhanssen, B, Peters, T, et al. Improvement in glucose metabolism after bariatric surgery: comparison of laparoscopic Roux-en-Y gastric bypass and laparoscopic sleeve gastrectomy: a prospective randomized trial. Ann Surg. 2009: 250, 234–241.CrossRefGoogle ScholarPubMed
Chambers, AP, Jessen, L, Ryan, KK, et al. Weight-independent changes in blood glucose homeostasis after gastric bypass or vertical sleeve gastrectomy in rats. Gastroenterology. 2011: 141, 950–958.CrossRefGoogle ScholarPubMed
Schauer, PR, Kashyap, SR, Wolski, K, et al. Bariatric surgery versus intensive medical therapy in obese patients with diabetes. N Engl J Med. 2012: 366, 1567–1576.CrossRefGoogle ScholarPubMed
Stemmer, K, Bielohuby, M, Grayson, BE, et al. Roux-en-Y gastric bypass surgery but not vertical sleeve gastrectomy decreases bone mass in male rats. Endocrinology. 2013: 154, 2015–2024.CrossRefGoogle Scholar
Grayson, BE, Schneider, KM, Woods, SC, Seeley, RJ. Improved rodent maternal metabolism but reduced intrauterine growth after vertical sleeve gastrectomy. Sci Transl Med. 2013: 5, 199ra112. doi: 10.1126/scitranslmed.3006505.CrossRefGoogle ScholarPubMed
Teitelman, M, Grotegut, C, Williams, N, Lewis, J. The impact of bariatric surgery on menstrual patterns. Obes Surg. 2006: 16, 1457.CrossRefGoogle ScholarPubMed
Rochester, D, Jain, A, Polotsky, AJ, et al. Partial recovery of luteal function after bariatric surgery in obese women. Fertil Steril. 2009: 92, 1410.CrossRefGoogle ScholarPubMed
Tan, O, Carr, BR. The impact of bariatric surgery on obesity-related infertility and in vitro fertilization outcomes. Semin Reprod Med. 2012: 30, 517–528. doi: 10.1055/s-0032-1328880.CrossRefGoogle ScholarPubMed
Johansson, K, Cnattingius, S, Näslund, I, et al. Outcomes of pregnancy after bariatric surgery. N Engl J Med. 2015: 372, 814–824. doi: 10.1056/NEJMoa1405789.CrossRefGoogle ScholarPubMed
Galazis, N, Docheva, N, Simillis, C, Nicolaides, KH. Maternal and neonatal outcomes in women undergoing bariatric surgery: a systematic review and meta-analysis. Eur J Obstet Gynecol Reprod Biol. 2014: 181, 45–53. doi: 10.1016/j.ejogrb.2014.07.015.CrossRefGoogle ScholarPubMed
Parker, MH, Berghella, V, Nijjar, JB. Bariatric surgery and associated adverse pregnancy outcomes among obese women. J Maternal-fetal Neonatal Med. 2015: 29, 1747–1750. doi: 10.3109/14767058.2015.1060214.CrossRefGoogle ScholarPubMed
Baker, RW, Osman, J, Bodnar, RJ. Differential actions of dopamine receptor antagonism in rats upon food intake elicited by either mercaptoacetate or exposure to a palatable high-fat diet. Pharmacol Biochem Behav. 2001: 69, 201–208.CrossRefGoogle ScholarPubMed
Gonzalez, I, Rubio, MA, Cordido, F, et al. Maternal and perinatal outcomes after bariatric surgery: a Spanish multicenter study. Obes Surg. 2015: 25, 436–442. doi: 10.1007/s11695-014-1387-7.CrossRefGoogle ScholarPubMed
Stefater, M, Pérez–Tilve, D, Chambers, AP, et al. Sleeve gastrectomy induces loss of weight and fat mass in obese rats, but does not affect leptin sensitivity. Gastroenterology. 2010: 138, 2426–2436 e2423.CrossRefGoogle Scholar
Wilson-Perez, HE, Chambers, AP, Sandoval, DA, Stefater, MA, Woods, SC, Benoit, SC, Seeley, RJ. The effect of vertical sleeve gastrectomy on food choice in rats. Int J Obesit. 2013: 37, 288–295.CrossRefGoogle ScholarPubMed
Parlee, SD, MacDougald, OA. Maternal nutrition and risk of obesity in offspring: the Trojan horse of developmental plasticity. Biochim Biophys Acta (BBA)-Mol Basis Dis. 2014: 1842, 495–506.CrossRefGoogle ScholarPubMed
Lactation, I. o. M. U. C. o. N. S. D. P. a. Nutrition During Lactation. Washington (DC): National Academies Press (US) Milk Volume 5 (1991).Google Scholar
Ameye, L, Devlieger, R, De Preter, V, et al. Bariatric surgery does not appear to affect women’s breast-milk composition. J Nutr. 2018: 148, 1096–1102. doi: 10.1093/jn/nxy085.Google Scholar
Garretto, D, Kim, YK, Quadro, L, et al. Vitamin A and beta-carotene in pregnant and breastfeeding post-bariatric women in an urban population. J Perinatal Med. 2019: 47, 183–189. doi: 10.1515/jpm-2018-0142.CrossRefGoogle Scholar
Ballard, O, Morrow, AL. Human milk composition: nutrients and bioactive factors. Pediatr Clin. 2013: 60, 49–74.Google ScholarPubMed
Lönnerdal, B. Nutritional and physiologic significance of human milk proteins. Am J Clin Nutr. 2003: 77, 1537S–1543S.CrossRefGoogle ScholarPubMed
Bachour, P, Yafawi, R, Jaber, F, Choueiri, E, Abdel-Razzak, Z. Effects of Smoking, Mother’s age, body mass index, and parity number on lipid, protein, and secretory immunoglobulin A concentrations of human milk. Breastfeed Med. 2011: 7, 179–188. doi: 10.1089/bfm.2011.0038.CrossRefGoogle ScholarPubMed
Rolls, BA, Gurr, MI, Van Duijvenvoorde, PM, Rolls, BJ, Rowe, EA. Lactation in lean and obese rats: effect of cafeteria feeding and of dietary obesity on milk composition. Physiol Behav. 1986: 38, 185–190. doi: 10.1016/0031-9384(86)90153-8.CrossRefGoogle ScholarPubMed
Grayson, BE, Gutierrez-Aguilar, R, Sorrell, JE, et al. Bariatric surgery emphasizes biological sex differences in rodent hepatic lipid handling. Biol Sex differences. 2017: 8, 4. doi: 10.1186/s13293-017-0126-x.CrossRefGoogle ScholarPubMed
Fields, DA, Demerath, EW. Relationship of insulin, glucose, leptin, IL-6 and TNF-alpha in human breast milk with infant growth and body composition. Pediatr Obesit. 2012: 7, 304–312. doi: 10.1111/j.2047-6310.2012.00059.x.CrossRefGoogle ScholarPubMed
Fields, DA, George, B, Williams, M, et al. Associations between human breast milk hormones and adipocytokines and infant growth and body composition in the first 6 months of life. Pediatr Obesit. 2017: 12 Suppl 1, 78–85. doi: 10.1111/ijpo.12182.CrossRefGoogle ScholarPubMed
Miralles, O, Sánchez, J, Palou, A, Picó, C. A physiological role of breast milk leptin in body weight control in developing infants. Obesity. 2006: 14, 1371–1377. doi: 10.1038/oby.2006.155.CrossRefGoogle ScholarPubMed
Uysal, FK, Önal, EE, Aral, YZ, Adam, B, Dilmen, U, Ardicolu, Y. Breast milk leptin: its relationship to maternal and infant adiposity. Clin Nutr. 2002: 21, 157–160. doi: 10.1054/clnu.2001.0525.CrossRefGoogle ScholarPubMed
Khodabakhshi, A, Ghayour-Mobarhan, M, Rooki, H, et al. Comparative measurement of ghrelin, leptin, adiponectin, EGF and IGF-1 in breast milk of mothers with overweight/obese and normal-weight infants. Eur J Clin Nutr. 2015: 69, 614–618. doi: 10.1038/ejcn.2014.205.CrossRefGoogle ScholarPubMed
Goropashnaya, AV, Herron, J, Sexton, M, et al. Relationships between plasma adiponectin and body fat distribution, insulin sensitivity, and plasma lipoproteins in Alaskan Yup’ik Eskimos: the Center for Alaska Native Health Research study. Metab: Clin Exp. 2009: 58, 22–29.CrossRefGoogle ScholarPubMed
Woo, JG, Guerrero, ML, Altaye, M, et al. Human milk adiponectin is associated with infant growth in two independent cohorts. Breastfeed Med: Off J Acad Breastfeed Med. 2009: 4, 101–109. doi: 10.1089/bfm.2008.0137.CrossRefGoogle ScholarPubMed
Spann, RA, Lawson, WJ, Bidwell, GL, et al. Rodent vertical sleeve gastrectomy alters maternal immune health and fetoplacental development. Clin Sci (Lond). 2018: 132, 295–312. doi: 10.1042/CS20171416.CrossRefGoogle ScholarPubMed
Weyermann, M, Brenner, H, Rothenbacher, D. Adipokines in human milk and risk of overweight in early childhood: a prospective cohort study. Epidemiology. 2007: 18, 722–729. doi: 10.1097/EDE.0b013e3181567ed4.CrossRefGoogle ScholarPubMed
Fujimori, M, França, EL, Fiorin, V, et al. Changes in the biochemical and immunological components of serum and colostrum of overweight and obese mothers. BMC Pregnancy Childb. 2015: 15, 166. doi: 10.1186/s12884-015-0574-4.CrossRefGoogle ScholarPubMed