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Published in: Maternal and Child Health Journal 6/2017

01-06-2017

Markers of Oxidative Stress in Human Milk do not Differ by Maternal BMI But are Related to Infant Growth Trajectories

Authors: Bridget E. Young, Zachary W. Patinkin, Laura Pyle, Becky de la Houssaye, Barbara S. Davidson, Sheela Geraghty, Ardythe L. Morrow, Nancy Krebs

Published in: Maternal and Child Health Journal | Issue 6/2017

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Abstract

Objective Obesity in adults is associated with inflammation and oxidative stress. Whether or not this phenotype is reflected in human milk (HM) composition, or may impact infant growth remains unknown. We investigated whether HM from overweight/obese (OW/Ob) mothers exhibited higher concentrations of inflammatory cytokines and markers of oxidative stress. We also correlated these bioactive components with infant growth patterns. Methods This was an observational cohort of 56 breastfeeding mothers and their infants [33 normal weight (NW) and 23 OW/Ob]. Infants were followed until 6 months of age and HM collected at 2-weeks and 4-months. Results Markers of oxidative stress, 8-hydroxy-deoxyguanosine (8OHdG) and 4-hydroxynonenol (HNE), decreased in HM over time (p < 0.001) and did not differ between NW and OW/Ob women. Concentrations of inflammatory cytokines, IL-6, IL-8, and TNF-α, were all inter-correlated (p < 0.001) but did not differ between NW and OW/Ob women. HM fat, protein, lactose, and total calories did not differ between NW and OW/Ob women. Infant growth patterns did not differ by group. In a model of infant weight-for-length-Z score trajectory, there was a significant interaction between both lactose and 8OHdG with maternal group: HM lactose and 8OHdG concentrations were both positively associated with increases in WLZ trajectory only among infants breastfed by OW/Ob mothers. Conclusions for Practice HM composition was relatively stable between NW and OW/Ob women. In exclusively breastfed infants, HM concentrations of lactose and 8OHdG, a marker of oxidative stress, may contribute to regulation of infant weight gain, especially among infants of OW/Ob women.
Literature
go back to reference Ahuja, S., Boylan, M., Hart, S., Roman-Shriver, C., Spallholz, J., Pence, B., & Sawyer, B. (2011). Glucose and insulin levels are increased in obese and overweight mothers’ breast-milk. Food and Nutrition Sciences, 2, 201–206.CrossRef Ahuja, S., Boylan, M., Hart, S., Roman-Shriver, C., Spallholz, J., Pence, B., & Sawyer, B. (2011). Glucose and insulin levels are increased in obese and overweight mothers’ breast-milk. Food and Nutrition Sciences, 2, 201–206.CrossRef
go back to reference Alexandre, V., Even, P. C., Larue-Achagiotis, C., Blouin, J. M., Blachier, F., Benamouzig, R., … & Davila, A. M. (2013). Lactose malabsorption and colonic fermentations alter host metabolism in rats. British Journal of Nutrition, 110(4), 625–631. doi:10.1017/S0007114512005557.CrossRefPubMed Alexandre, V., Even, P. C., Larue-Achagiotis, C., Blouin, J. M., Blachier, F., Benamouzig, R., … & Davila, A. M. (2013). Lactose malabsorption and colonic fermentations alter host metabolism in rats. British Journal of Nutrition, 110(4), 625–631. doi:10.​1017/​S000711451200555​7.CrossRefPubMed
go back to reference Barbosa, L., Butte, N. F., Villalpando, S., Wong, W. W., & Smith, E. O. (1997). Maternal energy balance and lactation performance of Mesoamerindians as a function of body mass index. The American Journal of Clinical Nutrition, 66(3), 575–583.PubMed Barbosa, L., Butte, N. F., Villalpando, S., Wong, W. W., & Smith, E. O. (1997). Maternal energy balance and lactation performance of Mesoamerindians as a function of body mass index. The American Journal of Clinical Nutrition, 66(3), 575–583.PubMed
go back to reference Beyerlein, A., & von Kries, R. (2011). Breastfeeding and body composition in children: Will there ever be conclusive empirical evidence for a protective effect against overweight? American Journal of Clinical Nutrition, 94(6 Suppl), 1772S–1775S. doi:10.3945/ajcn.110.000547.CrossRefPubMed Beyerlein, A., & von Kries, R. (2011). Breastfeeding and body composition in children: Will there ever be conclusive empirical evidence for a protective effect against overweight? American Journal of Clinical Nutrition, 94(6 Suppl), 1772S–1775S. doi:10.​3945/​ajcn.​110.​000547.CrossRefPubMed
go back to reference Boney, C. M., Verma, A., Tucker, R., & Vohr, B. R. (2005). Metabolic syndrome in childhood: Association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics, 115(3), e290–e296. doi:10.1542/peds.2004-1808.CrossRefPubMed Boney, C. M., Verma, A., Tucker, R., & Vohr, B. R. (2005). Metabolic syndrome in childhood: Association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics, 115(3), e290–e296. doi:10.​1542/​peds.​2004-1808.CrossRefPubMed
go back to reference Buyken, A. E., Karaolis-Danckert, N., Remer, T., Bolzenius, K., Landsberg, B., & Kroke, A. (2008). Effects of breastfeeding on trajectories of body fat and BMI throughout childhood., 16(2), 389–395. doi:10.1038/oby.2007.57. Buyken, A. E., Karaolis-Danckert, N., Remer, T., Bolzenius, K., Landsberg, B., & Kroke, A. (2008). Effects of breastfeeding on trajectories of body fat and BMI throughout childhood., 16(2), 389–395. doi:10.​1038/​oby.​2007.​57.
go back to reference Crume, T. L., Ogden, L. G., Mayer-Davis, E. J., Hamman, R. F., Norris, J. M., Bischoff, K. J., … Dabelea, D. (2012). The impact of neonatal breast-feeding on growth trajectories of youth exposed and unexposed to diabetes in utero: The EPOCH Study. International Journal of Obesity, 36(4), 529–534.CrossRefPubMedPubMedCentral Crume, T. L., Ogden, L. G., Mayer-Davis, E. J., Hamman, R. F., Norris, J. M., Bischoff, K. J., … Dabelea, D. (2012). The impact of neonatal breast-feeding on growth trajectories of youth exposed and unexposed to diabetes in utero: The EPOCH Study. International Journal of Obesity, 36(4), 529–534.CrossRefPubMedPubMedCentral
go back to reference Druet, C., Stettler, N., Sharp, S., Simmons, R. K., Cooper, C., Smith, G. D., … & Ong, K. K. (2012). Prediction of childhood obesity by infancy weight gain: An individual-level meta-analysis. Paediatric Perinatal Epidemiology, 26(1), 19–26.CrossRefPubMed Druet, C., Stettler, N., Sharp, S., Simmons, R. K., Cooper, C., Smith, G. D., … & Ong, K. K. (2012). Prediction of childhood obesity by infancy weight gain: An individual-level meta-analysis. Paediatric Perinatal Epidemiology, 26(1), 19–26.CrossRefPubMed
go back to reference Du, Y., Yang, M., Lee, S., Behrendt, C. L., Hooper, L. V., Saghatelian, A., & Wan, Y. (2012). Maternal western diet causes inflammatory milk and TLR2/4-dependent neonatal toxicity. Genes and Development, 26(12), 1306–1311.CrossRefPubMedPubMedCentral Du, Y., Yang, M., Lee, S., Behrendt, C. L., Hooper, L. V., Saghatelian, A., & Wan, Y. (2012). Maternal western diet causes inflammatory milk and TLR2/4-dependent neonatal toxicity. Genes and Development, 26(12), 1306–1311.CrossRefPubMedPubMedCentral
go back to reference Geraghty, S. R., Davidson, B. S., Warner, B. B., Sapsford, A. L., Ballard, J. L., List, B. A., … & Morrow, A. L. (2005). The development of a research human milk bank. Journal of Human Lactation, 21(1), 59–66.CrossRefPubMed Geraghty, S. R., Davidson, B. S., Warner, B. B., Sapsford, A. L., Ballard, J. L., List, B. A., … & Morrow, A. L. (2005). The development of a research human milk bank. Journal of Human Lactation, 21(1), 59–66.CrossRefPubMed
go back to reference Gorski, J. N., Dunn-Meynell, A. A., Hartman, T. G., & Levin, B. E. (2006). Postnatal environment overrides genetic and prenatal factors influencing offspring obesity and insulin resistance. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 291(3), R768–R778. doi:10.1152/ajpregu.00138.2006.PubMed Gorski, J. N., Dunn-Meynell, A. A., Hartman, T. G., & Levin, B. E. (2006). Postnatal environment overrides genetic and prenatal factors influencing offspring obesity and insulin resistance. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 291(3), R768–R778. doi:10.​1152/​ajpregu.​00138.​2006.PubMed
go back to reference Groer, M. W., & Shelton, M. M. (2009). Exercise is associated with elevated proinflammatory cytokines in human milk. J.Obstet.Gynecol.Neonatal Nurs., 38(1), 35–41.CrossRefPubMed Groer, M. W., & Shelton, M. M. (2009). Exercise is associated with elevated proinflammatory cytokines in human milk. J.Obstet.Gynecol.Neonatal Nurs., 38(1), 35–41.CrossRefPubMed
go back to reference He, T., Priebe, M. G., Harmsen, H. J., Stellaard, F., Sun, X., Welling, G. W., & Vonk, R. J. (2006). Colonic fermentation may play a role in lactose intolerance in humans. Journal of Nutrition, 136(1), 58–63.PubMed He, T., Priebe, M. G., Harmsen, H. J., Stellaard, F., Sun, X., Welling, G. W., & Vonk, R. J. (2006). Colonic fermentation may play a role in lactose intolerance in humans. Journal of Nutrition, 136(1), 58–63.PubMed
go back to reference Huh, J. Y., Son, D. J., Lee, Y., Lee, J., Kim, B., Lee, H. M., … & Chung, M. H. (2012). 8-Hydroxy-2-deoxyguanosine prevents plaque formation and inhibits vascular smooth muscle cell activation through Rac1 inactivation. Free Radical Biology and Medicine, 53(1), 109–121. doi:10.1016/j.freeradbiomed.2012.03.023.CrossRefPubMed Huh, J. Y., Son, D. J., Lee, Y., Lee, J., Kim, B., Lee, H. M., … & Chung, M. H. (2012). 8-Hydroxy-2-deoxyguanosine prevents plaque formation and inhibits vascular smooth muscle cell activation through Rac1 inactivation. Free Radical Biology and Medicine, 53(1), 109–121. doi:10.​1016/​j.​freeradbiomed.​2012.​03.​023.CrossRefPubMed
go back to reference Kalliomaki, M., Collado, M. C., Salminen, S., & Isolauri, E. (2008). Early differences in fecal microbiota composition in children may predict overweight. The American Journal of Clinical Nutrition, 87(3), 534–538.PubMed Kalliomaki, M., Collado, M. C., Salminen, S., & Isolauri, E. (2008). Early differences in fecal microbiota composition in children may predict overweight. The American Journal of Clinical Nutrition, 87(3), 534–538.PubMed
go back to reference Kim, D. H., Cho, I. H., Kim, H. S., Jung, J. E., Kim, J. E., Lee, K. H., … & Chung, M. H. (2006a). Anti-inflammatory effects of 8-hydroxydeoxyguanosine in LPS-induced microglia activation: Suppression of STAT3-mediated intercellular adhesion molecule-1 expression. Experimental and Molecular Medicine, 38(4), 417–427. doi:10.1038/emm.2006.49. Kim, D. H., Cho, I. H., Kim, H. S., Jung, J. E., Kim, J. E., Lee, K. H., … & Chung, M. H. (2006a). Anti-inflammatory effects of 8-hydroxydeoxyguanosine in LPS-induced microglia activation: Suppression of STAT3-mediated intercellular adhesion molecule-1 expression. Experimental and Molecular Medicine, 38(4), 417–427. doi:10.​1038/​emm.​2006.​49.
go back to reference Kim, H. S., Ye, S. K., Cho, I. H., Jung, J. E., Kim, D. H., Choi, S., … & Chung, M. H. (2006b). 8-hydroxydeoxyguanosine suppresses NO production and COX-2 activity via Rac1/STATs signaling in LPS-induced brain microglia. Free Radical Biology and Medicine, 41(9), 1392–1403. doi:10.1016/j.freeradbiomed.2006.07.018. Kim, H. S., Ye, S. K., Cho, I. H., Jung, J. E., Kim, D. H., Choi, S., … & Chung, M. H. (2006b). 8-hydroxydeoxyguanosine suppresses NO production and COX-2 activity via Rac1/STATs signaling in LPS-induced brain microglia. Free Radical Biology and Medicine, 41(9), 1392–1403. doi:10.​1016/​j.​freeradbiomed.​2006.​07.​018.
go back to reference Kirchner, S., Kieu, T., Chow, C., Casey, S., & Blumberg, B. (2010). Prenatal exposure to the environmental obesogen tributyltin predisposes multipotent stem cells to become adipocytes. Molecular endocrinology (Baltimore, Md.), 24(3), 526–539.CrossRef Kirchner, S., Kieu, T., Chow, C., Casey, S., & Blumberg, B. (2010). Prenatal exposure to the environmental obesogen tributyltin predisposes multipotent stem cells to become adipocytes. Molecular endocrinology (Baltimore, Md.), 24(3), 526–539.CrossRef
go back to reference Lam, P. M., Mistry, V., Marczylo, T. H., Konje, J. C., Evans, M. D., & Cooke, M. S. (2012). Rapid measurement of 8-oxo-7,8-dihydro-2′-deoxyguanosine in human biological matrices using ultra-high-performance liquid chromatography-tandem mass spectrometry. Free Radical Biology and Medicine, 52(10), 2057–2063.CrossRefPubMedPubMedCentral Lam, P. M., Mistry, V., Marczylo, T. H., Konje, J. C., Evans, M. D., & Cooke, M. S. (2012). Rapid measurement of 8-oxo-7,8-dihydro-2′-deoxyguanosine in human biological matrices using ultra-high-performance liquid chromatography-tandem mass spectrometry. Free Radical Biology and Medicine, 52(10), 2057–2063.CrossRefPubMedPubMedCentral
go back to reference Lawrence, R. A., Lawrence, R. M. (2011). Breastfeeding—a guide for the medical professional (7th ed.). Philadelphia: Elsevier Mosby. Lawrence, R. A., Lawrence, R. M. (2011). Breastfeeding—a guide for the medical professional (7th ed.). Philadelphia: Elsevier Mosby.
go back to reference Lee, S. H., Taek Han, S., Choi, S. W., Sung, S. Y., You, H. J., Ye, S. K., & Chung, M. H. (2009). Inhibition of Rac and Rac-linked functions by 8-oxo-2′-deoxyguanosine in murine macrophages. Free Radical Research, 43(1), 78–84. doi:10.1080/10715760802609432.CrossRefPubMed Lee, S. H., Taek Han, S., Choi, S. W., Sung, S. Y., You, H. J., Ye, S. K., & Chung, M. H. (2009). Inhibition of Rac and Rac-linked functions by 8-oxo-2′-deoxyguanosine in murine macrophages. Free Radical Research, 43(1), 78–84. doi:10.​1080/​1071576080260943​2.CrossRefPubMed
go back to reference Li, C., Kaur, H., Choi, W. S., Huang, T. T., Lee, R. E., & Ahluwalia, J. S. (2005). Additive interactions of maternal prepregnancy BMI and breast-feeding on childhood overweight. Obesity Research, 13(2), 362–371. doi:10.1038/oby.2005.48.CrossRefPubMed Li, C., Kaur, H., Choi, W. S., Huang, T. T., Lee, R. E., & Ahluwalia, J. S. (2005). Additive interactions of maternal prepregnancy BMI and breast-feeding on childhood overweight. Obesity Research, 13(2), 362–371. doi:10.​1038/​oby.​2005.​48.CrossRefPubMed
go back to reference Martin, L. J., Woo, J. G., Geraghty, S. R., Altaye, M., Davidson, B. S., Banach, W., … & Morrow, A. L. (2006). Adiponectin is present in human milk and is associated with maternal factors. The American Journal of Clinical Nutrition, 83(5), 1106–1111.PubMed Martin, L. J., Woo, J. G., Geraghty, S. R., Altaye, M., Davidson, B. S., Banach, W., … & Morrow, A. L. (2006). Adiponectin is present in human milk and is associated with maternal factors. The American Journal of Clinical Nutrition, 83(5), 1106–1111.PubMed
go back to reference Mayer-Davis, E. J., Rifas-Shiman, S. L., Zhou, L., Hu, F. B., Colditz, G. A., & Gillman, M. W. (2006). Breast-feeding and risk for childhood obesity: Does maternal diabetes or obesity status matter? Diabetes Care, 29(10), 2231–2237.CrossRefPubMedPubMedCentral Mayer-Davis, E. J., Rifas-Shiman, S. L., Zhou, L., Hu, F. B., Colditz, G. A., & Gillman, M. W. (2006). Breast-feeding and risk for childhood obesity: Does maternal diabetes or obesity status matter? Diabetes Care, 29(10), 2231–2237.CrossRefPubMedPubMedCentral
go back to reference Michalski, M. C., Calzada, C., Makino, A., Michaud, S., & Guichardant, M. (2008). Oxidation products of polyunsaturated fatty acids in infant formulas compared to human milk—a preliminary study. Molecular Nutrition & Food Research, 52(12), 1478–1485.CrossRef Michalski, M. C., Calzada, C., Makino, A., Michaud, S., & Guichardant, M. (2008). Oxidation products of polyunsaturated fatty acids in infant formulas compared to human milk—a preliminary study. Molecular Nutrition & Food Research, 52(12), 1478–1485.CrossRef
go back to reference Monteiro, P. O., & Victora, C. G. (2005). Rapid growth in infancy and childhood and obesity in later life—a systematic review. Obesity Reviews, 6(2), 143–154.CrossRefPubMed Monteiro, P. O., & Victora, C. G. (2005). Rapid growth in infancy and childhood and obesity in later life—a systematic review. Obesity Reviews, 6(2), 143–154.CrossRefPubMed
go back to reference Oben, J. A., Mouralidarane, A., Samuelsson, A. M., Matthews, P. J., Morgan, M. L., McKee, C., … & Taylor, P. D. (2010). Maternal obesity during pregnancy and lactation programs the development of offspring non-alcoholic fatty liver disease in mice. Journal of Hepatology, 52(6), 913–920.CrossRefPubMed Oben, J. A., Mouralidarane, A., Samuelsson, A. M., Matthews, P. J., Morgan, M. L., McKee, C., … & Taylor, P. D. (2010). Maternal obesity during pregnancy and lactation programs the development of offspring non-alcoholic fatty liver disease in mice. Journal of Hepatology, 52(6), 913–920.CrossRefPubMed
go back to reference Sederquist, B., Fernandez-Vojvodich, P., Zaman, F., & Savendahl, L. (2014). Recent research on the growth plate: Impact of inflammatory cytokines on longitudinal bone growth. Journal of Molecular Endocrinology, 53(1), T35–44. doi:10.1530/JME-14-0006. Sederquist, B., Fernandez-Vojvodich, P., Zaman, F., & Savendahl, L. (2014). Recent research on the growth plate: Impact of inflammatory cytokines on longitudinal bone growth. Journal of Molecular Endocrinology, 53(1), T35–44. doi:10.​1530/​JME-14-0006.
go back to reference Szlagatys-Sidorkiewicz, A., Zagierski, M., Jankowska, A., Luczak, G., Macur, K., Baczek, T., … Kaminska, B (2012). Longitudinal study of vitamins A, E and lipid oxidative damage in human milk throughout lactation. Early Human Development, 88(6), 421–424. doi:10.1016/j.earlhumdev.2011.10.007.CrossRefPubMed Szlagatys-Sidorkiewicz, A., Zagierski, M., Jankowska, A., Luczak, G., Macur, K., Baczek, T., … Kaminska, B (2012). Longitudinal study of vitamins A, E and lipid oxidative damage in human milk throughout lactation. Early Human Development, 88(6), 421–424. doi:10.​1016/​j.​earlhumdev.​2011.​10.​007.CrossRefPubMed
go back to reference Taveras, E. M., Rifas-Shiman, S. L., Sherry, B., Oken, E., Haines, J., Kleinman, K., … & Gillman, M. W. (2011). Crossing growth percentiles in infancy and risk of obesity in childhood. Archives of Pediatrics and Adolescent Medicine, 165(11), 993–998.CrossRefPubMed Taveras, E. M., Rifas-Shiman, S. L., Sherry, B., Oken, E., Haines, J., Kleinman, K., … & Gillman, M. W. (2011). Crossing growth percentiles in infancy and risk of obesity in childhood. Archives of Pediatrics and Adolescent Medicine, 165(11), 993–998.CrossRefPubMed
go back to reference Whitaker, R. C. (2004). Predicting preschooler obesity at birth: The role of maternal obesity in early pregnancy. Pediatrics, 114(1), e29–e36.CrossRefPubMed Whitaker, R. C. (2004). Predicting preschooler obesity at birth: The role of maternal obesity in early pregnancy. Pediatrics, 114(1), e29–e36.CrossRefPubMed
Metadata
Title
Markers of Oxidative Stress in Human Milk do not Differ by Maternal BMI But are Related to Infant Growth Trajectories
Authors
Bridget E. Young
Zachary W. Patinkin
Laura Pyle
Becky de la Houssaye
Barbara S. Davidson
Sheela Geraghty
Ardythe L. Morrow
Nancy Krebs
Publication date
01-06-2017
Publisher
Springer US
Published in
Maternal and Child Health Journal / Issue 6/2017
Print ISSN: 1092-7875
Electronic ISSN: 1573-6628
DOI
https://doi.org/10.1007/s10995-016-2243-2

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