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Consumption of sucrose, but not high fructose corn syrup, leads to increased adiposity and dyslipidaemia in the pregnant and lactating rat

Published online by Cambridge University Press:  19 December 2014

C. R. Toop ,
B. S. Muhlhausler ,
K. O’Dea  and
S. Gentili
C. R. Toop
Affiliation:
School of Pharmacy and Medical Sciences, University of South Australia, Adelaide, Australia
B. S. Muhlhausler
Affiliation:
FOODplus Research Centre, University of Adelaide, Adelaide, Australia
K. O’Dea
Affiliation:
School of Population Health, University of South Australia, Adelaide, Australia
S. Gentili*
Affiliation:
School of Pharmacy and Medical Sciences, University of South Australia, Adelaide, Australia
*
*Address for correspondence: S. Gentili, School of Pharmacy and Medical Sciences, University of South Australia, Adelaide 5001, Australia. (Email sheridan.gentili@unisa.edu.au)
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Abstract

Excess consumption of added sugars, including sucrose and high fructose corn syrup (HFCS-55), have been implicated in the global epidemics of obesity and type 2 diabetes. This study aimed to investigate and compare the impact of maternal consumption of sucrose or HFCS-55 during pregnancy and lactation on the metabolic health of the dam and her offspring at birth. Female Albino Wistar rats were given access to chow and water, in addition to a sucrose or HFCS-55 beverage (10% w/v) before, and during pregnancy and lactation. Maternal glucose tolerance was determined throughout the study, and a postmortem was conducted on dams following lactation, and on offspring within 24 h of birth. Sucrose and HFCS-55 consumption resulted in increased total energy intake compared with controls, however the increase from sucrose consumption was accompanied by a compensatory decrease in chow consumption. There was no effect of sucrose or HFCS-55 consumption on body weight, however sucrose consumption resulted in increased adiposity and elevated total plasma cholesterol in the dam, while HFCS-55 consumption resulted in increased plasma insulin and decreased plasma non-esterified fatty acids (NEFA). Maternal HFCS-55 consumption was associated with decreased relative liver weight and plasma NEFA in the offspring at birth. There was no effect of either treatment on pup weight at birth. These findings suggest that both sucrose and HFCS-55 consumption during pregnancy and lactation have the potential to impact negatively on maternal metabolic health, which may have adverse consequences for the long-term health of the offspring.

Keywords

adipose tissuehigh fructose corn syruplactationpregnancysucrose
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 6 , Issue 1 , February 2015 , pp. 38 - 46
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Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2014 

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References

1.Danaei, G, Finucane, MM, Lu, Y, et al. National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2·7 million participants. Lancet. 2011; 378, 31–40.CrossRefGoogle ScholarPubMed
2.Johnson, RK, Appel, LJ, Brands, M, et al. Dietary sugars intake and cardiovascular health: a scientific statement from the American Heart Association. Circulation. 2009; 120, 1011–1020.CrossRefGoogle Scholar
3.Fung, T, Malik, V, Rexrode, K, et al.Sweetened beverage consumption and risk of coronary heart disease in women. Am J Clin Nutr. 2009; 89, 1037–1042.CrossRefGoogle ScholarPubMed
4.Dhingra, R, Sullivan, L, Jacques, PF, et al. Soft drink consumption and risk of developing cardiometabolic risk factors and the metabolic syndrome in middle-aged adults in the community. Circulation. 2007; 116, 480–488.Google Scholar
5.Te Morenga, L, Mallard, S, Mann, J. Dietary sugars and body weight: systematic review and meta-analyses of randomised controlled trials and cohort studies. BMJ. 2013; 346, e7492.CrossRefGoogle Scholar
6.Willett, WC, Ludwig, DS. Science souring on sugar. BMJ. 2013; 346, e8077.CrossRefGoogle ScholarPubMed
7.McLennan, W, Podger, A. National Nutrition Survey Nutrient Intakes and Physical Measurements 1995. 1998. Australian Bureau of Statistics: Canberra.Google Scholar
8.Tappy, L, Lê, KA. Metabolic effects of fructose and the worldwide increase in obesity. Physiol Rev. 2010; 90, 23–46.Google Scholar
9.Douard, V, Ferraris, RP. The role of fructose transporters in diseases linked to excessive fructose intake. J Physiol. 2013; 591, 401–414.Google Scholar
10.Bizeau, ME, Pagliassotti, MJ. Hepatic adaptations to sucrose and fructose. Metabolism. 2005; 54, 1189–1201.CrossRefGoogle ScholarPubMed
11.Wei, Y, Wang, D, Topczewski, F, Pagliassotti, MJ. Fructose-mediated stress signaling in the liver: implications for hepatic insulin resistance. J Nutr Biochem. 2007; 18, 1–9.Google Scholar
12.Lustig, RH. Fructose: it’s ‘alcohol without the buzz’. Adv Nutr. 2013; 4, 226–235.CrossRefGoogle ScholarPubMed
13.Regnault, TRH, Gentili, S, Sarr, O, Toop, CR, Sloboda, DM. Fructose, pregnancy and later life impacts. Clin Exp Pharmacol Physiol. 2013; 40, 824–837.CrossRefGoogle ScholarPubMed
14.Bray, G, Nielsen, S, Popkin, B. Consumption of high-fructose corn syrup in beverages may play a role in the epidemic of obesity. Am J Clin Nutr. 2004; 79, 537–543.CrossRefGoogle ScholarPubMed
15.Alfaradhi, M, Ozanne, S. Developmental programming in response to maternal over-nutrition. Front Genet. 2011; 2, 27.Google Scholar
16.McMillen, IC, Robinson, JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev. 2005; 85, 571–633.CrossRefGoogle ScholarPubMed
17.Chen, LW, Hu, FB, Yeung, E, Willett, W, Zhang, CL. Prospective study of pre-gravid sugar-sweetened beverage consumption and the risk of gestational diabetes mellitus. Diabetes Care. 2009; 32, 2236–2241.Google Scholar
18.Nelson, SM, Matthews, P, Poston, L. Maternal metabolism and obesity: modifiable determinants of pregnancy outcome. Hum Reprod Update. 2010; 16, 255–275.CrossRefGoogle ScholarPubMed
19.Siega-Riz, AM, Bodnar, LM, Savitz, DA. What are pregnant women eating? Nutrient and food group differences by race. Am J Obstet Gynecol. 2002; 186, 480–486.CrossRefGoogle ScholarPubMed
20.Borgen, I, Aamodt, G, Harsem, N, et al.Maternal sugar consumption and risk of preeclampsia in nulliparous Norwegian women. Eur J Clin Nutr. 2012; 66, 920–925.CrossRefGoogle ScholarPubMed
21.Englund-Ögge, L, Brantsæter, AL, Haugen, M, et al. Association between intake of artificially sweetened and sugar-sweetened beverages and preterm delivery: a large prospective cohort study. Am J Clin Nutr. 2012; 96, 552–559.CrossRefGoogle ScholarPubMed
22.Phelan, S, Hart, C, Phipps, M, et al. Maternal behaviors during pregnancy impact offspring obesity risk. Exp Diabetes Res. 2011; 2011, 9.CrossRefGoogle ScholarPubMed
23.Goran, MI, Dumke, K, Bouret, SG, et al.The obesogenic effect of high fructose exposure during early development. Nat Rev Endocrinol. 2013; 9, 494–500.Google Scholar
24.Sloboda, DM, Li, M, Patel, R, et al.Early life exposure to fructose and offspring phenotype: implications for long term metabolic homeostasis. J Obes. 2014; 2014, 10.Google Scholar
25.Vickers, MH, Clayton, ZE, Yap, C, Sloboda, DM. Maternal fructose intake during pregnancy and lactation alters placental growth and leads to sex-specific changes in fetal and neonatal endocrine function. Endocrinology. 2011; 152, 1378–1387.CrossRefGoogle ScholarPubMed
26.Mukai, Y, Kumazawa, M, Sato, S. Fructose intake during pregnancy up-regulates the expression of maternal and fetal hepatic sterol regulatory element-binding protein-1c in rats. Endocrine. 2012; 44, 79–86.CrossRefGoogle ScholarPubMed
27.Mukai, Y, Ozaki, H, Serita, Y, Sato, S. Maternal fructose intake during pregnancy modulates hepatic and hypothalamic AMP-activated protein kinase signaling in gender-specific manner in offspring. Clin Exp Pharmacol Physiol. 2014; 41, 331–337.CrossRefGoogle Scholar
28.Rodríguez, L, Panadero, MI, Roglans, N, et al. Fructose during pregnancy affects maternal and fetal leptin signaling. J Nutr Biochem. 2013; 24, 1709–1716.Google Scholar
29.Samuelsson, AM, Matthews, PA, Jansen, E, Taylor, PD, Poston, L. Sucrose feeding in mouse pregnancy leads to hypertension, and sex-linked obesity and insulin resistance in female offspring. Front Physiol. 2013; 4, 14.CrossRefGoogle ScholarPubMed
30.Jen, KL, Rochon, C, Zhong, S, Whitcomb, L. Fructose and sucrose feeding during pregnancy and lactation in rats changes maternal and pup fuel metabolism. J Nutr. 1991; 121, 1999–2005.Google Scholar
31.Soria, A, Chicco, A, Mocchiutti, N, et al. A sucrose-rich diet affects triglyceride metabolism differently in pregnant and nonpregnant rats and has negative effects on fetal growth. J Nutr. 1996; 126, 2481–2486.CrossRefGoogle ScholarPubMed
32.D’Alessandro, ME, Oliva, ME, Ferreira, MR, et al. Sucrose-rich feeding during rat pregnancy-lactation and/or after weaning alters glucose and lipid metabolism in adult offspring. Clin Exp Pharmacol Physiol. 2012; 39, 623–629.CrossRefGoogle ScholarPubMed
33.D’Alessandro, ME, Oliva, ME, Fortino, MA, Chicco, A. Maternal sucrose-rich diet and fetal programming: changes in hepatic lipogenic and oxidative enzymes and glucose homeostasis in adult offspring. Food Funct. 2014; 5, 446–453.CrossRefGoogle ScholarPubMed
34.Taylor, PD, Poston, L. Developmental programming of obesity in mammals. Exp Physiol. 2007; 92, 287–298.Google Scholar
35.Light, HR, Tsanzi, E, Gigliotti, J, Morgan, K, Tou, JC. The type of caloric sweetener added to water influences weight gain, fat mass, and reproduction in growing Sprague-Dawley female rats. Exp Biol Med (Maywood). 2009; 234, 651–661.CrossRefGoogle ScholarPubMed
36.Sheludiakova, A, Rooney, K, Boakes, R. Metabolic and behavioural effects of sucrose and fructose/glucose drinks in the rat. Eur J Nutr. 2011; 51, 445–454.CrossRefGoogle ScholarPubMed
37.Bergheim, I, Weber, S, Vos, M, et al. Antibiotics protect against fructose-induced hepatic lipid accumulation in mice: role of endotoxin. J Hepatol. 2008; 48, 983–992.CrossRefGoogle ScholarPubMed
38.Lindqvist, A, Baelemans, A, Erlanson-Albertsson, C. Effects of sucrose, glucose and fructose on peripheral and central appetite signals. Regul Pept. 2008; 150, 26–32.CrossRefGoogle ScholarPubMed
39.Page, K, Chan, O, Arora, J, et al. Effects of fructose vs glucose on regional cerebral blood flow in brain regions involved with appetite and reward pathways. JAMA. 2013; 309, 63–70.Google Scholar
40.Butte, NF. Carbohydrate and lipid metabolism in pregnancy: normal compared with gestational diabetes mellitus. Am J Clin Nutr. 2000; 71, 1256S–1261SS.CrossRefGoogle ScholarPubMed
41.Lee, VM, Szepesi, B, Hansen, RJ. Absence of a Generalized Disaccharide Effect in Adult Female Rats. J Nutr. 1986; 116, 1555–1560.CrossRefGoogle ScholarPubMed
42.Michaelis, OE, Nace, CS, Szepesi, B. Demonstration of a specific metabolic effect of dietary disaccharides in the rat. J Nutr. 1975; 105, 1186–1191.Google Scholar
43.Soria, A, D’Alessandro, ME, Lombardo, YB. Duration of feeding on a sucrose-rich diet determines metabolic and morphological changes in rat adipocytes. J Appl Physiol (1985). 2001; 91, 2109–2116.Google Scholar
44.Shoelson, SE, Lee, J, Goldfine, AB. Inflammation and insulin resistance. J Clin Invest. 2006; 116, 1793–1801.CrossRefGoogle ScholarPubMed
45.Cahova, M, Dankova, H, Palenickova, E, Papackova, Z, Kazdova, L. The opposite effects of high-sucrose and high-fat diet on fatty acid oxidation and very low density lipoprotein secretion in rat model of metabolic syndrome. J Nutr Metab. 2012; 2012, 757205.CrossRefGoogle ScholarPubMed
46.Su, Q, Tsai, J, Xu, E, et al. Apolipoprotein B100 acts as a molecular link between lipid-induced endoplasmic reticulum stress and hepatic insulin resistance. Hepatology. 2009; 50, 77–84.Google Scholar
47.Lustig, RH. Fructose: metabolic, hedonic, and societal parallels with ethanol. J Am Diet Assoc. 2010; 110, 1307–1321.CrossRefGoogle ScholarPubMed
48.Crescenzo, R, Bianco, F, Coppola, P, et al. The effect of high-fat-high-fructose diet on skeletal muscle mitochondrial energetics in adult rats. Eur J Nutr. 2014; doi:10.1007/s00394-014-0699-7.Google Scholar
49.McMillen, IC, MacLaughlin, SM, Muhlhausler, BS, et al. Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition. Basic Clin Pharmacol Toxicol. 2008; 102, 82–89.Google Scholar
50.Guo, Y, Zhang, X, Huang, J, et al. Relationships between hematopoiesis and hepatogenesis in the midtrimester fetal liver characterized by dynamic transcriptomic and proteomic profiles. PLoS One. 2009; 4, e7641.Google Scholar
51.Kinoshita, T, Miyajima, A. Cytokine regulation of liver development. Biochim Biophys Acta. 2002; 1592, 303–312.CrossRefGoogle ScholarPubMed
52.Mikkola, HK, Orkin, SH. The journey of developing hematopoietic stem cells. Development. 2006; 133, 3733–3744.Google Scholar