|Year : 2019 | Volume
| Issue : 1 | Page : 17-22
Maternal consumption of sucrose during lactation may program metabolic dysfunction in young offspring
Nkiru A Katchy, Pearl A Okeke, Eghosa E Iyare
Reproductive and Developmental Programming Research Group, Department of Physiology, Faculty of Basic Medical Sciences, College of Medicine, University of Nigeria,Enugu, Nigeria
|Date of Web Publication||13-Sep-2019|
Miss. Nkiru A Katchy
Reproductive and Developmental Programming Research Group, Department of Physiology, Faculty of Basic Medical Sciences, College of Medicine, University of Nigeria, Enugu Campus, Enugu
Source of Support: None, Conflict of Interest: None
Background: It is well established that the consumption of sugars by both young and old, males and females, has tremendously increased over the past decades. This increased consumption is without prejudice to the physiological state of the body. There is evidence to suggest a correlation between the excessive consumption of these sugars and their adverse metabolic effects. Aim: The aim of this study was carried out to investigate the effect of maternal consumption of sucrose during lactation on some metabolic indices in young offspring of the rat. Methods: Fourteen female albino Wistar rats weighing were used for this study and were randomly assigned into two groups (sucrose group and control group) at delivery. Water and 30% (w/v) sucrose solutions from plastic bottles were made with tap water and administered during lactation until weaning. At postnatal day 42, offspring of sucrose-fed rats showed a statistically significant decrease (P < 0.05) in body weight and food intake when compared with control. The female offspring showed a statistically significant increase (P < 0.05) in liver weight index, total cholesterol, and triglycerides and a significant decrease in high-density lipoprotein (HDL) and insulin values (P < 0.05) when compared with control. The male offspring showed a statistically significant increase (P < 0.05) in the oral glucose tolerance test, total cholesterol, triglycerides, low-density lipoprotein values and a significant decrease in pancreatic weight, HDL, and insulin concentration when compared with control. Conclusion: This study suggests that maternal consumption of sucrose during lactation may contribute to the onset of metabolic dysfunction in the young adult offspring.
Keywords: Developmental programming, lactation, metabolic dysfunction, offspring, sucrose
|How to cite this article:|
Katchy NA, Okeke PA, Iyare EE. Maternal consumption of sucrose during lactation may program metabolic dysfunction in young offspring. Niger J Exp Clin Biosci 2019;7:17-22
|How to cite this URL:|
Katchy NA, Okeke PA, Iyare EE. Maternal consumption of sucrose during lactation may program metabolic dysfunction in young offspring. Niger J Exp Clin Biosci [serial online] 2019 [cited 2020 Jan 22];7:17-22. Available from: http://www.njecbonline.org/text.asp?2019/7/1/17/266835
| Introduction|| |
Sugars are important component of the modern diet. One of the most important of these is sucrose commonly referred to as table sugar. The intake of refined sugars has increased markedly over the past two decades and is consumed in high quantity among adolescents and adults., The World Health Organization recommended that added sugars should contribute <10% and preferably <5% or roughly 25 g/day to total energy intake. Despite this, a significant proportion of the population continues to consume considerably over this amount.,
Evidence from numerous studies demonstrates a correlation between the excessive consumption of these sweeteners and their adverse metabolic effects.,
The concept of developmental origins of adult disease often called “developmental programming,” proposes that environmental factors or conditions, including maternal nutrition experienced in utero and during early postnatal life, can elicit permanent metabolic and physiological modifications in individuals, giving rise to enhanced susceptibility to develop diseases later in life. Feeding conditions likely constitute one of the most influential parameters on the health of the adult. Thus, diet manipulation in mothers during critical developmental periods (such as gestation and/or the early postnatal) has been used to identify their contribution to obesity, diabetes, and other metabolic disorders development in offspring. Consumption of excess added sugars, that is, sugars/syrups added to foods and beverages as sweeteners have been implicated in the development of a number of metabolic abnormalities, including insulin resistance, dyslipidemia, and obesity, in both humans and animals.,, Several studies have shown that maternal consumption of sucrose during pregnancy and lactation programs the development of hypertension, sex-linked obesity, insulin resistance, hypertriglyceridemia, dyslipidemia, and higher adiposity in the offspring later in life.,, Diets high in simple sugars have been reported to exert a high glycemic index and are a major cause of metabolic syndrome. This study, therefore, was aimed at determining whether maternal consumption of sucrose during lactation may program the development of metabolic dysfunction in the young adult offspring.
| Methods|| |
A total of 16 female albino Wistar rats weighing 180–210 g were used for this study. The animals were purchased from the Faculty of Basic Medical Sciences' Animal House, University of Nigeria, Enugu Campus. They were weighed, randomly assigned into metallic cages, kept in a room where a 12-h light/dark cycle was maintained and were allowed free access to livestock feed (Vital Feeds, Nigeria Ltd), and tap water ad libitum throughout the experiment. The rats were allowed for 1 week to acclimatize before the commencement of the study.
The estrous cycles were monitored, and male rats of proven fertility were introduced into the cages of the female rats that were expected to get into the estrous phase within 12 h to allow for mating. Day 1 of pregnancy was taken as the day sperm were seen in the vaginal smear of the rats. All rats were fed normal rat chow throughout pregnancy.
At delivery, dams were randomly assigned into two groups (control group and sucrose group), and the pups were culled to 8 pups/dam to prevent overnutrition and/or undernutrition of the pups. Dams in the control group were given tap water to drink throughout lactation, whereas dams in the sucrose groups were given 30% (w/v) sucrose solutions to drink throughout lactation as shown in [Table 1].
Weaning occurred at postnatal day (PND) 21. Pups were removed from their mothers and group-housed, with free access to chow and water.
All procedures used in this study conformed with the guiding principles for research involving animals as recommended by the Declaration of Helsinki, and the guiding principles in the care and use of animals and were approved by the Institutional Ethical Committee.
Measurement of body weights, hepatic, and pancreatic weight
Offspring body weights were measured weekly from PND 1 to PND 42 while food consumption was measured from PND 21 to PND 42. Hepatic and pancreatic weights were measured on PND 42 and used for the calculation of the weight indices. The digital electronic compact balance was used for all measurements.
Determination of oral glucose tolerance test
The offspring were deprived of food for 12 h (overnight) and were then given 2 g/kg body weight as glucose solution orally. The tail blood samples were collected at 0, 30, 60, and 120 min time interval. The blood glucose levels were determined with the aid of one-touch basic glucometer.
Blood Sample collection and serum preparations
At PND 42, blood samples of the five male and five female offspring (n = 10) per group were collected by cardiac puncture into specimen bottles and allowed to clot and separated by centrifugation. Serum was used for the determination of lipid profile and insulin levels.
The levels of cholesterol and triglyceride were assayed for using enzymatic colorimetric diagnostic kits obtained from Randox Laboratories, UK, in which, the glycerol phosphate oxidase method  was employed. High-density lipoprotein cholesterol (HDL-C) was determined according to the method of Burstein et al., and low-density lipoprotein (LDL) cholesterol was calculated as: LDL (mg/dL) = (total cholesterol-HDL + total triglyceride/5 while very low-density lipoprotein (VLDL)-cholesterol was estimated as VLDL (mg/dL) = (triglyceride/5). Serum insulin was measured using enzyme-linked immunosorbent assay (ELISA) using insulin ELISA kit.
Data were expressed as mean ± standard error of the mean and the values were analyzed using the Student's t-test. Differences between groups were considered statistically significant at P < 0.05.
| Results|| |
Effect of maternal sucrose consumption on offspring weekly body weight
Maternal sucrose consumption during lactation caused a progressive decrease (P < 0.05) in the postnatal body weights of the offspring beginning from the preweaning PND 14 to postweaning PND 42 [Figure 1].
|Figure 1: Body weight of offspring of rats that consumed water (control) and sucrose during lactation. *Significantly different when compared with control|
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Effect of maternal sucrose consumption on offspring food intake
Maternal sucrose consumption during lactation also caused a progressive decrease (P < 0.05) in the postweaning food consumption of the offspring beginning from the 1st week postweaning (PND 28) to the 3rd week postweaning (PND 42) [Figure 2].
|Figure 2: Food intake of offspring of rats that consumed water (control) and sucrose during lactation. *Significantly different when compared with control|
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Effect of maternal sucrose consumption on offspring liver weight index
[Figure 3] shows the offspring liver weight index of control and sucrose groups for female and male offspring. The control group was significantly (P < 0.05) lower than the sucrose group in the female offspring.
|Figure 3: Liver weight index of male and female offspring in control and sucrose groups. *Significantly greater when compared with control|
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Effect of maternal sucrose consumption on offspring pancreatic weight index
[Figure 4] shows the effect of maternal sucrose consumption on female and male offspring pancreatic weight index. There was no significant difference in the weight index of the female offspring when compared with control while a significant decrease (P < 0.05) was observed in the male offspring when compared with control.
|Figure 4: Pancreatic weight index of male and female offspring of control and sucrose groups. *Significantly lower when compared with control|
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Effect of maternal sucrose consumption on offspring oral glucose tolerance test
[Figure 5] shows the oral glucose tolerance test (OGTT) values for the control and sucrose groups. The offspring of the sucrose group maintained significantly (P < 0.05) higher values in blood glucose level at 0, 30, 60, and 90 min than the control group.
|Figure 5: Trend of oral glucose tolerance test of offspring of rats in control and sucrose. *Significantly higher when compared with control|
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Effect of maternal sucrose consumption on offspring lipid profiles
[Figure 6] and [Figure 7] show comparative results for lipid profiles between the control group and the sucrose group in female and male offspring, respectively. The sucrose group was significantly (P < 0.05) higher than the control for total cholesterol, and total triglyceride in the female offspring but significantly (P < 0.05) lower than the control for HDL. Sucrose group was significantly (P < 0.05) higher than the control values for total cholesterol, total triglyceride, and LDL but significantly (P < 0.05) lower than the control values for HDL in the male offspring.
|Figure 6: Lipid profile of female offspring of control and sucrose groups. *Significantly different when compared with control|
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|Figure 7: Lipid profile of male offspring of control and sucrose groups. *Significantly different when compared with control|
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Effect of maternal sucrose consumption on offspring insulin concentration
[Figure 8] and [Figure 9] show the effect of sucrose on insulin level in female and male offspring of albino Wistar rats fed with sucrose water. It shows that the sucrose control group was significantly (P < 0.05) lower than the normal control group in insulin level for both male and female offspring.
|Figure 8: Insulin level of male offspring of rats that consumed water and sucrose during lactation. *Significantly different when compared with control|
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|Figure 9: Insulin level of female offspring of rats that consumed water and sucrose during lactation. *Significantly different when compared with control|
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| Discussion|| |
The intake of refined sugars has increased markedly over the past two decades and consumption of excess added sugars as sweeteners have been implicated in the development of some metabolic abnormalities.,
Diet manipulation in mothers during critical developmental periods (such as gestation, lactation, and/or the early postnatal) could have harmful effects which have been used to identify risk factors in obesity, diabetes, and other metabolic disorders in the offspring. Therefore, the composition of the maternal diet can have profound effects on the metabolism and the growth of the offspring.
Measurement of anthropometric indices such as total body weight and weight changes of tissues is necessary because weight changes of these tissues are useful measures of their pathological condition. This study showed that maternal sucrose consumption during lactation caused a decrease in body weight of the offspring of rats when compared with control. It is beyond dispute that pup growth during lactation is directly related to maternal food intake. Other studies that have investigated the effects of maternal sucrose consumption during pregnancy and lactation ,, reported increased body weight of offspring which is dependent on both sex and age. The discrepancies between these studies and the present study may be explained by differences in maternal sugar consumption, exposure window, and the age at which offspring were evaluated. Reduced weaning weight of offspring may suggest reduced milk production during lactation because the need for milk production is met through dietary energy and body tissue mobilization. In this study, milk production and consumption were not determined in response to sucrose feeding. Coffey et al. had reported that lactating multiparous sows fed with fructose have been shown to have reduced milk production and reduced milk fat percentage. Hence, low weaning weight of offspring observed in this study could be as a result of fructose moiety in sucrose. Therefore, it is reasonable to assume that impaired growth in the suckling phase for offspring from sucrose-fed rats is the result of a reduction in the quantity of nutrients available from milk to support growth due to decreased maternal food intake. Hence, impaired offspring growth observed in the offspring born to sucrose group predicts a higher risk of metabolic syndrome in later life of the offspring due to macronutrient imbalances which can increase the risk of metabolic disorders development in offspring.
The liver is one of the largest glandular organs in the body that serves as a metabolic powerhouse for the processing of nutrients, absorption of lipids, and glycogen storage to maintain energy levels. An increase in the relative weight of the liver was observed in the female offspring of sucrose-fed rats even though their mean body weights were decreased when compared with control. This could be attributed to increased triglyceride accumulation leading to enlarged liver.
OGTT measures the body's ability to metabolize glucose and determines the body's response to glucose loading. In the present study, maternal consumption of sucrose caused a significant increase in fasting blood glucose concentration in the offspring. Following glucose loading, the blood glucose in the sucrose group similarly decreased with time, compared with control, suggesting that glucose tolerance was not impaired when compared with control. This may suggest that the 30% sucrose solution consumed during lactation caused metabolic stress during lactation that was sufficient to precipitate the fasting hyperglycemia observed in the offspring.
The glucose tolerance observed in this study is in line with the work of Jen et al., who reported that the in vivo glucose tolerance was not impaired in rats fed with fructose or sucrose diets. On the contrary, the result of this work is in contrast with the report of Samuelsson et al. who reported that glucose intolerance was evident in female offspring of sucrose-fed dams, with a prolonged recovery phase in the glucose tolerance test and that there were no apparent differences in the glucose response curves in male offspring. The discrepancies between studies may be explained by differences in methods of administration, maternal sugar consumption, environmental conditions, exposure window, and the age at which offspring were evaluated.
Dyslipidemia is a common manifestation in diabetes mellitus cases and is associated with greater risk of atherosclerosis characterized by increased levels of triglycerides, VLDL and LDL, the presence of small dense LDL particles, and decreased HDL levels. Sucrose administration increased total cholesterol, triglyceride in both sexes while the increase in LDL was significant in female offspring and an increase in VLDL and HDL in male offspring. An increase in lipid indices as sucrose concentrations increases has been reported by Salau et al. Association between sucrose intake and cholesterol level has been established., When sucrose is consumed, it is broken down to glucose and fructose. Absorbed fructose is converted to lipogenic precursors, leading to increase in plasma triglyceride levels.,
Insulin is the main pancreatic hormone which closely regulates glucose in the blood. In normal individuals, the response to increased plasma glucose level is an increase in the secretion of insulin from β-cells of the pancreatic islets. This increase in circulating insulin levels leads to the stimulation of glucose transport into peripheral tissues while inhibiting hepatic gluconeogenesis. Maternal sucrose administration during lactation decreased the insulin level of male and female offspring when compared with control. This decrease in insulin level observed could be as a result of the suppressive effect of sucrose on the β-cells of the pancreatic islets during lactation which might be the reason for the fasting hyperglycemia.
The results of the present study may suggest that maternal consumption of sucrose during lactation may contribute to the onset of metabolic dysfunction in the young adult offspring. Hence, it may have great effect on the metabolism and the growth of the offspring.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Nikpartow N, Danyliw AD, Whiting SJ, Lim HJ, Vatanparast H. Beverage consumption patterns of Canadian adults aged 19 to 65 years. Public Health Nutr 2012;15:2175-84.
Jensen BW, Nichols M, Allender S, de Silva-Sanigorski A, Millar L, Kremer P, et al
. Consumption patterns of sweet drinks in a population of Australian children and adolescents (2003–2008). BMC Public Health 2012;12:771.
World Health Organization. Guideline: Sugars Intake for Adults and Children. Geneva, Switzerland: World Health Organization; 2015.
Johnson DB, Bruemmer B, Lund AE, Evens CC, Mar CM. Impact of school district sugar-sweetened beverage policies on student beverage exposure and consumption in middle schools. J Adolesc Health 2009;45:S30-7.
Stanhope KL, Havel PJ. Endocrine and metabolic effects of consuming beverages sweetened with fructose, glucose, sucrose, or high-fructose corn syrup. Am J Clin Nutr 2008;88:1733S-7S.
Malik VS, Hu FB. Sweeteners and risk of obesity and type 2 diabetes: The role of sugar-sweetened beverages. Curr Diab Rep 2012;12:195-203.
Barouki R, Gluckman PD, Grandjean P, Hanson M, Heindel JJ. Developmental origins of non-communicable disease: Implications for research and public health. Environ Health 2012;11:42.
Alzamendi A, Castrogiovanni D, Gaillard RC, Spinedi E, Giovambattista A. Increased male offspring's risk of metabolic-neuroendocrine dysfunction and overweight after fructose-rich diet intake by the lactating mother. Endocrinology 2010;151:4214-23.
Clayton ZE, Vickers MH, Bernal A, Yap C, Sloboda DM. Early life exposure to fructose alters maternal, fetal and neonatal hepatic gene expression and leads to sex-dependent changes in lipid metabolism in rat offspring. PLoS One 2015;10:e0141962.
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;5:446-53.
Armitage JA, Taylor PD, Poston L. Experimental models of developmental programming: Consequences of exposure to an energy rich diet during development. J Physiol 2005;565:3-8.
Kendig MD, Ekayanti W, Stewart H, Boakes RA, Rooney K. Metabolic effects of access to sucrose drink in female rats and transmission of some effects to their offspring. PLoS One 2015;10:e0131107.
D'Alessandro ME, Oliva ME, Ferreira MR, Selenscig D, Lombardo YB, Chicco A, 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;39:623-9.
Schulze MB, Liu S, Rimm EB, Manson JE, Willett WC, Hu FB, et al.
Glycemic index, glycemic load, and dietary fiber intake and incidence of type 2 diabetes in younger and middle-aged women. Am J Clin Nutr 2004;80:348-56.
Bellinger L, Sculley DV, Langley-Evans SC. Exposure to undernutrition in fetal life determines fat distribution, locomotor activity and food intake in ageing rats. Int J Obes (Lond) 2006;30:729-38.
Trinder P. Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Ann Clin Biochem 1996;6:24-7.
Burstein M, Scholnick HR, Morfin R. Rapid method for the isolation of lipoproteins from human serum by precipitation with polyanions. J Lipid Res 1970;11:583-95.
Regnault TR, Gentili S, Sarr O, Toop CR, Sloboda DM. Fructose, pregnancy and later life impacts. Clin Exp Pharmacol Physiol 2013;40:824-37.
Usoh IF, Akpanyuyng EO. Leaves extracts of gongronema latifolium and ocimum gratissimum offer synergy on organ weights alleviation and pancreatic resurgence against streptozotocin diabetic rats. J Innov Pharmaceut Biol Sci 2015;2:522-36.
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.
Coffey MT, Yates JA, Combs GE. Effects of feeding sows fat or fructose during late gestation and lactation. J Anim Sci 1987;65:1249-56.
Islam MA, Akhtar MA, Khan MR, Hossain MS, Alam AH, Ibne-Wahed MI, et al.
Oral glucose tolerance test (OGTT) in normal control and glucose induced hyperglycemic rats with Coccinia cordifolia
L. and Catharanthus roseus
L. Pak J Pharm Sci 2009;22:402-4.
Jen KL, Rochon C, Zhong SB, Whitcomb L. Fructose and sucrose feeding during pregnancy and lactation in rats changes maternal and pup fuel metabolism. J Nutr 1991;121:1999-2005.
Arca M, Montali A, Valiante S, Campagna F, Pigna G, Paoletti V, et al.
Usefulness of atherogenic dyslipidemia for predicting cardiovascular risk in patients with angiographically defined coronary artery disease. Am J Cardiol 2007;100:1511-6.
Salau BA, Olooto WE, Adebayo OL, Ajani EO, Odufuwa KT, Olowookere JO. Sucrose diet elevates cardiovascular risk factors in male albino rats. Int J Biol Chem 2012;6:61-8.
Albrink MJ, Ullrich IH. Interaction of dietary sucrose and fiber on serum lipids in healthy young men fed high carbohydrate diets. Am J Clin Nutr 1986;43:419-28.
Richards EG, Grundy SM, Cooper K. Influence of plasma triglycerides on lipoprotein patterns in normal subjects and in patients with coronary artery disease. Am J Cardiol 1989;63:1214-20.
Dekker MJ, Su Q, Baker C, Rutledge AC, Adeli K. Fructose: A highly lipogenic nutrient implicated in insulin resistance, hepatic steatosis, and the metabolic syndrome. Am J Physiol Endocrinol Metab 2010;299:E685-94.
Chong MF, Fielding BA, Frayn KN. Mechanisms for the acute effect of fructose on postprandial lipemia. Am J Clin Nutr 2007;85:1511-20.
Cheatham B, Kahn CR. Insulin action and the insulin signaling network. Endocr Rev 1995;16:117-42.
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