The Investigation of The Metabolic Effect of High Salt or Western Diet During Pregnancy and Lactation on Rat Dams and Postnatal Offspring Rats
Year 2024,
, 484 - 493, 28.06.2024
Meryem Elif Öztürk
,
Nurcan Yabancı Ayhan
Abstract
Objective: This study investigated the metabolic effect of maternal high-salt and western low-protein diets during pregnancy and lactation periods on rat dams and adult offspring.
Methods: Female rat dams were divided into four groups and fed with a 1% high salt diet, a Western low-protein diet (high fat and sugar and low protein), or a 1% high salt/western low-protein combined diet (WS) during pregnancy and lactation. Afterward, 95 female and male offspring were divided into groups and fed with those diets until 18 weeks of age. The mothers’ and offspring rats' body weights and chow intake were recorded periodically. At 18 weeks of age, blood samples were collected from the offspring. Their blood lipid profiles, leptin, and insulin levels were analyzed.
Results: Rat dams had similar weight changes during pregnancy and lactation. Rats exposed to the Western low-protein and WS diet during pregnancy, lactation, and/or postweaning had lower body weights than the control group. Male adult offspring from control dams and fed high salt were heavier and had higher LDL cholesterol than controls. However, rats from high salt dams and fed a high salt diet had lower body weights than the control group. Plasma insulin and leptin of male rats were not significantly different. Female offspring fed Western low-protein and WS diet in the fetal period or in early childhood had significantly low insulin. However, female rats exposed to Western low-protein and WS diets during pregnancy, lactation, and postweaning had similar insulin to control rats.
Conclusion: Maintaining the maternal diet after lactation prevents the detrimental effect of a low-protein diet on insulin levels. Anti-obesity mechanism may develop in offspring exposed to a high salt diet during the fetal period against salt intake in later life.
Ethical Statement
The experimental procedures were approved by the Ankara University Animal Experimentation Ethics Committee under protocol number 2018-17-114.
Thanks
We are grateful to animal lab director and Mahmut Bodur for their help
References
- Wu G, Bazer FW, Cudd TA, Meininger CJ, Spencer TE. Maternal nutrition and fetal development. J Nutr. 2004;134(9):2169-2172. DOI:10.1093/jn/134.9.2169
- Segovia SA, Vickers MH, Harrison CJ, Patel R, Gray C, Reynolds CM. Maternal high-fat and high-salt diets have differential programming effects on metabolism in adult male rat offspring. Front Nutr. 2018;5. DOI:10.3389/fnut.2018.00001
- Pruis MGM, Lendvai Á, Bloks VW, Zwier MV, Baller JFW, de Bruin A, Groen AK, Plösch T. Maternal western diet primes non‐alcoholic fatty liver disease in adult mouse offspring. Acta Physiol. 2013;210: 215–227. DOI:10.1111/apha.12197
- Grech A, Sui Z, Rangan A, Simpson SJ, Coogan SCP, Raubenheimer D. Macronutrient (im)balance drives energy intake in an obesogenic food environment: An ecological analysis. Obesity 2022;30: 2156–2166. DOI:10.1002/oby.23578
- Graudal N, Jürgens G, Baslund B, Alderman MH. Compared with usual sodium intake, low- and excessive-sodium diets are associated with increased mortality: a meta-analysis. Am. J. Hypertens. 2014;27:1129–1137. DOI:10.1093/ajh/hpu028
- Donovan DS, Solomon CG, Seely EW, Williams GH, Simonson DC. Effect of sodium intake on insulin sensitivity. Am. J. Physiol. Endocrinol. Metab. 1993;264: E730–E734. DOI:10.1152/ajpendo.1993.264.5.E730
- Ohta Y, Tsuchihashi T, Kiyohara K, Oniki H. High salt intake promotes a decline in renal function in hypertensive patients: a 10-year observational study. Hypertens. Res. 2012;36: 172–176. DOI:10.1038/hr.2012.155
- Lanaspa MA, Kuwabara M, Andres-Hernando A, Li N, Cicerchi C, Jensen T, Orlicky DJ, Roncal-Jimenez CA, Ishimoto T, Nakagawa T, Rodriguez-Iturbe B, MacLean PS, Johnson RJ. High salt intake causes leptin resistance and obesity in mice by stimulating endogenous fructose production and metabolism. PNAS. 2018;115: 3138–3143. DOI:10.1073/pnas.1713837115
- Huang M, Li X, Ren L, Huang L, Pan J, Yao J, Du Lili, Chen Dunjin, Chen Jingsi. Maternal high salt-diet increases offspring’s blood pressure with dysfunction of NO/PKGI signaling pathway in heart tissue. Gynecol. Obstet. Clin. Med. 2022;2(2):69–75. DOI:10.1016/j.gocm.2022.03.001
- Dilli D, Oğuz ŞS, Dilmen U. Fetal programlanma. Türkiye Çocuk Hastalıkları Dergisi. 2010;4(4): 245-252 (Turkish).
- Savitikadi P, Gogulothu R, Ismail A, Reddy GB, Reddy VS. Combined prenatal to postnatal protein restriction augments protein quality control processes and proteolysis in the muscle of rat offspring. J Nutr Biochem. 2023;114:109273. DOI:10.1016/j.jnutbio.2023.109273
- Rodríguez-González GL, De Los Santos S, Méndez-Sánchez D, Reyes-Castro LA, Ibáñez CA, Canto P, et al. High-fat diet consumption by male rat offspring of obese mothers exacerbates adipose tissue hypertrophy and metabolic alterations in adult life. Br J Nutr. 2023;130(5):783-792. DOI:10.1017/S0007114522003737
- Tajaddini A, Kendig MD, Prates KV, Westbrook RF, Morris MJ. Male rat offspring are more impacted by maternal obesity induced by cafeteria diet than females-additive effect of postweaning diet. Int J Mol Sci. 2022;23(3):1442. DOI:10.3390/ijms23031442
- Niu L, Han DW, Xu RL, Han B, Zhou X, Wu HW, Li SH, Qu CX, Liu M. A high-sugar high-fat diet induced metabolic syndrome shows some symptoms of Alzheimer’s disease in rats. J Nutr Health Aging. 2016; 20(5): 509-513. DOI:10.1007/s12603-015-0601-1
- She M, Deng X, Guo Z, Laudon M, Hu Z, Liao D, Hu X, Luo Y, Shen Q, Su Z, Yin W. NEU-P11, a novel melatonin agonist, inhibits weight gain and improves insulin sensitivity in high-fat/high-sucrose-fed rats. Pharmacol Res. 2009;59(4):248-253.
DOI:10.1016/j.phrs.2009.01.005.
- Alexandre-Gouabau MC, David-Sochard A, Royer AL, Parnet P, Paillé V. Moderate high caloric maternal diet impacts dam breast milk metabotype and offspring lipidome in a sex-specific manner. int J Mol Sci. 2020; 21(15): 5428. DOI:10.3390/ijms21155428
- Merle L, Person O, Bonnet P, Grégoire S, Soubeyre V, Grosmaitre X, Jarriault D. Maternal high fat high sugar diet disrupts olfactory behavior but not mucosa sensitivity in the offspring. Psychoneuroendocrinology 2019;104: 249-258. DOI:10.1016/j.psyneuen.2019.02.005
- National Research Council [NRC]. Control of Diets in Laboratory Animal Experiments. 1978; National Academy Press, Washington, DC.
- National Research Council (NRC) Subcommittee on Laboratory Animal Nutrition. Nutrient Requirements of Laboratory Animals: Fourth Revised Edition, 1995; National Academies Press, Washington (DC).
- Brito PD, Ramos CF, Passos MC, Moura EG. Adaptive changes in thyroid function of female rats fed a high-fat and low-protein diet during gestation and lactation. Braz J Med Biol. 2006;39(6): 809-816. DOI:10.1590/s0100-879x2006000600015
- Ding Y, Lv J, Mao C, Zhang H, Wang A, Zhu L, Zhu H, Xu Z et al. High-salt diet during pregnancy and angiotensin-related cardiac changes. J. Hypertens. 2010; 28(6): 1290-1297 DOI:10.1097/HJH.0b013e328337da8f
- Gray C, Al-Dujaili EA, Sparrow AJ, Gardiner SM, Craigon J, Welham SJ, Gardner DS. Excess maternal salt intake produces sex-specific hypertension in offspring: putative roles for kidney and gastrointestinal sodium handling. PloS One. 2013;8(8): e72682. DOI:10.1371/journal.pone.0072682
- Stocher DP, Klein CP, Saccomori AB, August PM, Martins NC, Couto PRG, Hagen MEK, Matté C. Maternal high-salt diet alters redox state and mitochondrial function in newborn rat offspring’s brain. Br J Nutr. 2018; 119(9): 1003-1011. DOI:10.1017/S0007114518000235
- Lagisz M, Blair H, Kenyon P, Uller T, Raubenheimer D, Nakagawa, S. Little appetite for obesity: Meta-analysis of the effects of maternal obesogenic diets on offspring food intake and body mass in rodents. Int J Obes (Lond) (2005). 2015; 39(12): 1669–1678. DOI:10.1038/ijo.2015.160
- Coupé B, Grit I, Darmaun D, Parnet P. The timing of “catch-up growth” affects metabolism and appetite regulation in male rats born with intrauterine growth restriction. Am J Physiol Regul Integr Comp Physiol. 2009;297(3): 813-824. DOI:10.1152/ajpregu.00201.2009
- Friedman JM. Leptin and the regulation of body weight. Keio J Med. 2011;60(1): 1-9. DOI:10.2302/kjm.60.1
- Loh K, Zhang L, Brandon A, Wang Q, Begg D, Qi Y, Fu M, Kulkarni R, Teo J, Baldock P, Brüning JC, Cooney G, Neely GG, Herzog H. Insulin controls food intake and energy balance via NPY neurons. Mol. Metab. 2017;6: 574–584. DOI:10.1016/j.molmet.2017.03.013
- Bolhuis DP, Costanzo A, Newman LP, Keast RS. Salt promotes passive overconsumption of dietary fat in humans. J Nutr, 2015; 146(4): 838-845. DOI:10.3945/jn.115.226365.
- Bouhlal S, Issanchou S, Nicklaus S. The impact of salt, fat and sugar levels on toddler food intake. Br J Nutr. 2011; 105(4): 645-653. DOI:10.1017/S0007114510003752
- Pitynski-Miller D, Ross M, Schmill M, Schambow R, Fuller T, Flynn FW, Skinner DC. A high salt diet inhibits obesity and delays puberty in the female rat. Int J Obes (Lond). 2017; 41(11): 1685-1692. DOI:10.1038/ijo.2017.154.
- Ibrahim H, Saad A, Habeeb W, Abdel-raouf S. Effect of high salt diet on bone in adult male albino rats. MJMR. 2020;31: 136–140. DOI:10.21608/MJMR.2022.217549
- Coimbra TM, Francescato HD, Balbi AP, Marin EC, Costa RS. Renal development and blood pressure in offspring from dams submitted to high-sodium intake during pregnancy and lactation. Int. J. Nephrol. 2012;2012: 1–5. DOI:10.1155/2012/919128
- Mean salt intake in adults aged 25 years and older in the Americas, 1990-2019. ENLACE Data Portal. Pan American Health Organization, 2023. [Internet] Available online at https://www.paho.org/en/enlace/salt-intake.
- Ritz E. Salt—friend or foe? Nephrol Dial Transplant. 2005;21: 2052–2056. DOI:10.1016/S0140-6736(13)61104-6
- Bingham S, McNeil NI, Cummings JH. The diet of individuals: A study of a randomly-chosen cross section of British adults in a Cambridgeshire village. British Journal of Nutrition. 1981;45:23–35. DOI:10.1079/bjn19810074.
- Ma Y, He FJ, MacGregor GA. High Salt Intake: independent risk factor for obesity? Hypertension 2015;66:843–849. DOI:10.1161/HYPERTENSIONAHA.115.05948
- Larsen SC, Ängquist L, Sørensen TI, Heitmann BL. 24h urinary sodium excretion and subsequent change in weight, waist circumference and body composition. Plos One 2013;8(7):e69689. DOI:10.1371/journal.pone.0069689
- Klop B, Elte J, Cabezas M. Dyslipidemia in obesity: mechanisms and potential targets. Nutrients 2013;5: 1218–1240. DOI:10.3390/nu5041218
- Gohar EY, De Miguel C, Obi IE, Daugherty EM, Hyndman KA, Becker BK, Jin C, Sedaka R, Johnston JG, Liu P, Speed JS, Mitchell T, Kriegel AJ, Pollock JS, Pollock DM. Acclimation to a high-salt diet is sex dependent. J Am Heart Assoc. 2022;11(5):e020450. DOI:10.1161/JAHA.120.020450.
- Miñana-Solis M, Escobar C. Post-weaning protein malnutrition in the rat produces short and long term metabolic impairment, in contrast to earlier and later periods. Int J Biol Sci. 2008;4(6):422–432. DOI:10.7150/ijbs.4.422
- O'Donnell M, Mente A, Rangarajan S, McQueen MJ, Wang X, Liu L, Yan H, Lee SF, Mony P, Devanath A, Rosengren A, Lopez-Jaramillo P, Diaz R, Avezum A, Lanas F, Yusoff K, Iqbal R, Ilow R, Mohammadifard N, Gulec S, Yusufali AH, Kruger L, Yusuf R, Chifamba J, Kabali C, Dagenais G, Lear SA, Teo K, Yusuf S; PURE Investigators. Urinary sodium and potassium excretion, mortality, and cardiovascular events. NEJM. 2014; 371(7): 612-623. DOI:10.1056/NEJMoa1311889
- Padilha BM, Ferreira RC, Bueno NB, Tassitano RM, Holanda LS, Vasconcelos SML, Cabral PC. Association between blood cholesterol and sodium intake in hypertensive women with excess weight. Medicine. 2018;97:e0371. DOI:10.1097/MD.0000000000010371
- Wang C, Huang Z, Yu K, Ding R, Ye K, Dai C, Xu X, Zhou G, Li C. High-salt diet has a certain impact on protein digestion and gut microbiota: a sequencing and proteome combined study. Front. microbiol. 2017;8:1838. DOI:10.3389/fmicb.2017.01838
- Vourakis M, Mayer G, Rousseau G. The role of gut microbiota on cholesterol metabolism in atherosclerosis. Int. J. Mol. Sci. 2021;22:8074. DOI:10.3390/ijms22158074
- Gosby AK, Stanton LM, Maloney CA, Thompson M, Briody J, Baxter RC Bryson JM, Denyer GS, Caterson ID. Postnatal nutrition alters body composition in adult offspring exposed to maternal protein restriction. Br. J. Nutr. 2008;101: 1878–1884. DOI:10.1017/S0007114508135851
- Yokomizo H, Inoguchi T, Sonoda N, Sakaki Y, Maeda Y, Inoue T, Hirata E, Takei R, Ikeda N, Fujii M, Fukuda K, Sasaki H, Takayanagi R. Maternal high-fat diet induces insulin resistance and deterioration of pancreatic β-cell function in adult offspring with sex differences in mice. Am J Physiol Endocrinol. 2014; 306(10): 1163-1175. DOI:10.1152/ajpendo.00688.2013
- Berleze KJ, Müller AP, Schweigert ID, Longoni A, Sordi F, de Assis AM, Rotta LN, de Souza DO, Perry ML. Gestational and postnatal low protein diet alters insulin sensitivity in female rats. EBM. 2009;234: 1437–1444. DOI:10.3181/0903-RM-111
- Jayasooriya AP, Mathai ML, Walker LL, Begg DP, Denton DA, Cameron-Smith D, Egan GF, McKinley MJ, Rodger PD, Sinclair AJ, Wark JD, Weisinger HS, Jois M, Weisinger RS. Mice lacking angiotensin converting enzyme have increased energy expenditure, with reduced fat mass and improved glucose clearance. PNAS 2008;105(18):6531-6536. DOI:10.1073/pnas.0802690105
- Coelho MS, Passadore MD, Gasparetti AL, Bibancos T, Prada PO, Furukawa LL, Furukawa LN, Fukui RT, Casarini DE, Saad MJ, Luz J, Chiavegatto S, Dolnikoff MS, Heimann JC. High-or low salt diet from weaning to adulthood: effect on body weight, food intake and energy balance in rats. Nutr Metab Cardiovasc Dis. 2006;16(2): 148-155. DOI:10.1016/j.numecd.2005.09.001
- Piecha G, Koleganova N, Ritz E, Müller A, Fedorova OV, Bagrov AY, et al. (2012). High salt intake causes adverse fetal programming—vascular effects beyond blood pressure. Nephrol Dial Transpl. 2012; 27(9): 3464-3476. DOI:10.1093/ndt/gfs027
Year 2024,
, 484 - 493, 28.06.2024
Meryem Elif Öztürk
,
Nurcan Yabancı Ayhan
References
- Wu G, Bazer FW, Cudd TA, Meininger CJ, Spencer TE. Maternal nutrition and fetal development. J Nutr. 2004;134(9):2169-2172. DOI:10.1093/jn/134.9.2169
- Segovia SA, Vickers MH, Harrison CJ, Patel R, Gray C, Reynolds CM. Maternal high-fat and high-salt diets have differential programming effects on metabolism in adult male rat offspring. Front Nutr. 2018;5. DOI:10.3389/fnut.2018.00001
- Pruis MGM, Lendvai Á, Bloks VW, Zwier MV, Baller JFW, de Bruin A, Groen AK, Plösch T. Maternal western diet primes non‐alcoholic fatty liver disease in adult mouse offspring. Acta Physiol. 2013;210: 215–227. DOI:10.1111/apha.12197
- Grech A, Sui Z, Rangan A, Simpson SJ, Coogan SCP, Raubenheimer D. Macronutrient (im)balance drives energy intake in an obesogenic food environment: An ecological analysis. Obesity 2022;30: 2156–2166. DOI:10.1002/oby.23578
- Graudal N, Jürgens G, Baslund B, Alderman MH. Compared with usual sodium intake, low- and excessive-sodium diets are associated with increased mortality: a meta-analysis. Am. J. Hypertens. 2014;27:1129–1137. DOI:10.1093/ajh/hpu028
- Donovan DS, Solomon CG, Seely EW, Williams GH, Simonson DC. Effect of sodium intake on insulin sensitivity. Am. J. Physiol. Endocrinol. Metab. 1993;264: E730–E734. DOI:10.1152/ajpendo.1993.264.5.E730
- Ohta Y, Tsuchihashi T, Kiyohara K, Oniki H. High salt intake promotes a decline in renal function in hypertensive patients: a 10-year observational study. Hypertens. Res. 2012;36: 172–176. DOI:10.1038/hr.2012.155
- Lanaspa MA, Kuwabara M, Andres-Hernando A, Li N, Cicerchi C, Jensen T, Orlicky DJ, Roncal-Jimenez CA, Ishimoto T, Nakagawa T, Rodriguez-Iturbe B, MacLean PS, Johnson RJ. High salt intake causes leptin resistance and obesity in mice by stimulating endogenous fructose production and metabolism. PNAS. 2018;115: 3138–3143. DOI:10.1073/pnas.1713837115
- Huang M, Li X, Ren L, Huang L, Pan J, Yao J, Du Lili, Chen Dunjin, Chen Jingsi. Maternal high salt-diet increases offspring’s blood pressure with dysfunction of NO/PKGI signaling pathway in heart tissue. Gynecol. Obstet. Clin. Med. 2022;2(2):69–75. DOI:10.1016/j.gocm.2022.03.001
- Dilli D, Oğuz ŞS, Dilmen U. Fetal programlanma. Türkiye Çocuk Hastalıkları Dergisi. 2010;4(4): 245-252 (Turkish).
- Savitikadi P, Gogulothu R, Ismail A, Reddy GB, Reddy VS. Combined prenatal to postnatal protein restriction augments protein quality control processes and proteolysis in the muscle of rat offspring. J Nutr Biochem. 2023;114:109273. DOI:10.1016/j.jnutbio.2023.109273
- Rodríguez-González GL, De Los Santos S, Méndez-Sánchez D, Reyes-Castro LA, Ibáñez CA, Canto P, et al. High-fat diet consumption by male rat offspring of obese mothers exacerbates adipose tissue hypertrophy and metabolic alterations in adult life. Br J Nutr. 2023;130(5):783-792. DOI:10.1017/S0007114522003737
- Tajaddini A, Kendig MD, Prates KV, Westbrook RF, Morris MJ. Male rat offspring are more impacted by maternal obesity induced by cafeteria diet than females-additive effect of postweaning diet. Int J Mol Sci. 2022;23(3):1442. DOI:10.3390/ijms23031442
- Niu L, Han DW, Xu RL, Han B, Zhou X, Wu HW, Li SH, Qu CX, Liu M. A high-sugar high-fat diet induced metabolic syndrome shows some symptoms of Alzheimer’s disease in rats. J Nutr Health Aging. 2016; 20(5): 509-513. DOI:10.1007/s12603-015-0601-1
- She M, Deng X, Guo Z, Laudon M, Hu Z, Liao D, Hu X, Luo Y, Shen Q, Su Z, Yin W. NEU-P11, a novel melatonin agonist, inhibits weight gain and improves insulin sensitivity in high-fat/high-sucrose-fed rats. Pharmacol Res. 2009;59(4):248-253.
DOI:10.1016/j.phrs.2009.01.005.
- Alexandre-Gouabau MC, David-Sochard A, Royer AL, Parnet P, Paillé V. Moderate high caloric maternal diet impacts dam breast milk metabotype and offspring lipidome in a sex-specific manner. int J Mol Sci. 2020; 21(15): 5428. DOI:10.3390/ijms21155428
- Merle L, Person O, Bonnet P, Grégoire S, Soubeyre V, Grosmaitre X, Jarriault D. Maternal high fat high sugar diet disrupts olfactory behavior but not mucosa sensitivity in the offspring. Psychoneuroendocrinology 2019;104: 249-258. DOI:10.1016/j.psyneuen.2019.02.005
- National Research Council [NRC]. Control of Diets in Laboratory Animal Experiments. 1978; National Academy Press, Washington, DC.
- National Research Council (NRC) Subcommittee on Laboratory Animal Nutrition. Nutrient Requirements of Laboratory Animals: Fourth Revised Edition, 1995; National Academies Press, Washington (DC).
- Brito PD, Ramos CF, Passos MC, Moura EG. Adaptive changes in thyroid function of female rats fed a high-fat and low-protein diet during gestation and lactation. Braz J Med Biol. 2006;39(6): 809-816. DOI:10.1590/s0100-879x2006000600015
- Ding Y, Lv J, Mao C, Zhang H, Wang A, Zhu L, Zhu H, Xu Z et al. High-salt diet during pregnancy and angiotensin-related cardiac changes. J. Hypertens. 2010; 28(6): 1290-1297 DOI:10.1097/HJH.0b013e328337da8f
- Gray C, Al-Dujaili EA, Sparrow AJ, Gardiner SM, Craigon J, Welham SJ, Gardner DS. Excess maternal salt intake produces sex-specific hypertension in offspring: putative roles for kidney and gastrointestinal sodium handling. PloS One. 2013;8(8): e72682. DOI:10.1371/journal.pone.0072682
- Stocher DP, Klein CP, Saccomori AB, August PM, Martins NC, Couto PRG, Hagen MEK, Matté C. Maternal high-salt diet alters redox state and mitochondrial function in newborn rat offspring’s brain. Br J Nutr. 2018; 119(9): 1003-1011. DOI:10.1017/S0007114518000235
- Lagisz M, Blair H, Kenyon P, Uller T, Raubenheimer D, Nakagawa, S. Little appetite for obesity: Meta-analysis of the effects of maternal obesogenic diets on offspring food intake and body mass in rodents. Int J Obes (Lond) (2005). 2015; 39(12): 1669–1678. DOI:10.1038/ijo.2015.160
- Coupé B, Grit I, Darmaun D, Parnet P. The timing of “catch-up growth” affects metabolism and appetite regulation in male rats born with intrauterine growth restriction. Am J Physiol Regul Integr Comp Physiol. 2009;297(3): 813-824. DOI:10.1152/ajpregu.00201.2009
- Friedman JM. Leptin and the regulation of body weight. Keio J Med. 2011;60(1): 1-9. DOI:10.2302/kjm.60.1
- Loh K, Zhang L, Brandon A, Wang Q, Begg D, Qi Y, Fu M, Kulkarni R, Teo J, Baldock P, Brüning JC, Cooney G, Neely GG, Herzog H. Insulin controls food intake and energy balance via NPY neurons. Mol. Metab. 2017;6: 574–584. DOI:10.1016/j.molmet.2017.03.013
- Bolhuis DP, Costanzo A, Newman LP, Keast RS. Salt promotes passive overconsumption of dietary fat in humans. J Nutr, 2015; 146(4): 838-845. DOI:10.3945/jn.115.226365.
- Bouhlal S, Issanchou S, Nicklaus S. The impact of salt, fat and sugar levels on toddler food intake. Br J Nutr. 2011; 105(4): 645-653. DOI:10.1017/S0007114510003752
- Pitynski-Miller D, Ross M, Schmill M, Schambow R, Fuller T, Flynn FW, Skinner DC. A high salt diet inhibits obesity and delays puberty in the female rat. Int J Obes (Lond). 2017; 41(11): 1685-1692. DOI:10.1038/ijo.2017.154.
- Ibrahim H, Saad A, Habeeb W, Abdel-raouf S. Effect of high salt diet on bone in adult male albino rats. MJMR. 2020;31: 136–140. DOI:10.21608/MJMR.2022.217549
- Coimbra TM, Francescato HD, Balbi AP, Marin EC, Costa RS. Renal development and blood pressure in offspring from dams submitted to high-sodium intake during pregnancy and lactation. Int. J. Nephrol. 2012;2012: 1–5. DOI:10.1155/2012/919128
- Mean salt intake in adults aged 25 years and older in the Americas, 1990-2019. ENLACE Data Portal. Pan American Health Organization, 2023. [Internet] Available online at https://www.paho.org/en/enlace/salt-intake.
- Ritz E. Salt—friend or foe? Nephrol Dial Transplant. 2005;21: 2052–2056. DOI:10.1016/S0140-6736(13)61104-6
- Bingham S, McNeil NI, Cummings JH. The diet of individuals: A study of a randomly-chosen cross section of British adults in a Cambridgeshire village. British Journal of Nutrition. 1981;45:23–35. DOI:10.1079/bjn19810074.
- Ma Y, He FJ, MacGregor GA. High Salt Intake: independent risk factor for obesity? Hypertension 2015;66:843–849. DOI:10.1161/HYPERTENSIONAHA.115.05948
- Larsen SC, Ängquist L, Sørensen TI, Heitmann BL. 24h urinary sodium excretion and subsequent change in weight, waist circumference and body composition. Plos One 2013;8(7):e69689. DOI:10.1371/journal.pone.0069689
- Klop B, Elte J, Cabezas M. Dyslipidemia in obesity: mechanisms and potential targets. Nutrients 2013;5: 1218–1240. DOI:10.3390/nu5041218
- Gohar EY, De Miguel C, Obi IE, Daugherty EM, Hyndman KA, Becker BK, Jin C, Sedaka R, Johnston JG, Liu P, Speed JS, Mitchell T, Kriegel AJ, Pollock JS, Pollock DM. Acclimation to a high-salt diet is sex dependent. J Am Heart Assoc. 2022;11(5):e020450. DOI:10.1161/JAHA.120.020450.
- Miñana-Solis M, Escobar C. Post-weaning protein malnutrition in the rat produces short and long term metabolic impairment, in contrast to earlier and later periods. Int J Biol Sci. 2008;4(6):422–432. DOI:10.7150/ijbs.4.422
- O'Donnell M, Mente A, Rangarajan S, McQueen MJ, Wang X, Liu L, Yan H, Lee SF, Mony P, Devanath A, Rosengren A, Lopez-Jaramillo P, Diaz R, Avezum A, Lanas F, Yusoff K, Iqbal R, Ilow R, Mohammadifard N, Gulec S, Yusufali AH, Kruger L, Yusuf R, Chifamba J, Kabali C, Dagenais G, Lear SA, Teo K, Yusuf S; PURE Investigators. Urinary sodium and potassium excretion, mortality, and cardiovascular events. NEJM. 2014; 371(7): 612-623. DOI:10.1056/NEJMoa1311889
- Padilha BM, Ferreira RC, Bueno NB, Tassitano RM, Holanda LS, Vasconcelos SML, Cabral PC. Association between blood cholesterol and sodium intake in hypertensive women with excess weight. Medicine. 2018;97:e0371. DOI:10.1097/MD.0000000000010371
- Wang C, Huang Z, Yu K, Ding R, Ye K, Dai C, Xu X, Zhou G, Li C. High-salt diet has a certain impact on protein digestion and gut microbiota: a sequencing and proteome combined study. Front. microbiol. 2017;8:1838. DOI:10.3389/fmicb.2017.01838
- Vourakis M, Mayer G, Rousseau G. The role of gut microbiota on cholesterol metabolism in atherosclerosis. Int. J. Mol. Sci. 2021;22:8074. DOI:10.3390/ijms22158074
- Gosby AK, Stanton LM, Maloney CA, Thompson M, Briody J, Baxter RC Bryson JM, Denyer GS, Caterson ID. Postnatal nutrition alters body composition in adult offspring exposed to maternal protein restriction. Br. J. Nutr. 2008;101: 1878–1884. DOI:10.1017/S0007114508135851
- Yokomizo H, Inoguchi T, Sonoda N, Sakaki Y, Maeda Y, Inoue T, Hirata E, Takei R, Ikeda N, Fujii M, Fukuda K, Sasaki H, Takayanagi R. Maternal high-fat diet induces insulin resistance and deterioration of pancreatic β-cell function in adult offspring with sex differences in mice. Am J Physiol Endocrinol. 2014; 306(10): 1163-1175. DOI:10.1152/ajpendo.00688.2013
- Berleze KJ, Müller AP, Schweigert ID, Longoni A, Sordi F, de Assis AM, Rotta LN, de Souza DO, Perry ML. Gestational and postnatal low protein diet alters insulin sensitivity in female rats. EBM. 2009;234: 1437–1444. DOI:10.3181/0903-RM-111
- Jayasooriya AP, Mathai ML, Walker LL, Begg DP, Denton DA, Cameron-Smith D, Egan GF, McKinley MJ, Rodger PD, Sinclair AJ, Wark JD, Weisinger HS, Jois M, Weisinger RS. Mice lacking angiotensin converting enzyme have increased energy expenditure, with reduced fat mass and improved glucose clearance. PNAS 2008;105(18):6531-6536. DOI:10.1073/pnas.0802690105
- Coelho MS, Passadore MD, Gasparetti AL, Bibancos T, Prada PO, Furukawa LL, Furukawa LN, Fukui RT, Casarini DE, Saad MJ, Luz J, Chiavegatto S, Dolnikoff MS, Heimann JC. High-or low salt diet from weaning to adulthood: effect on body weight, food intake and energy balance in rats. Nutr Metab Cardiovasc Dis. 2006;16(2): 148-155. DOI:10.1016/j.numecd.2005.09.001
- Piecha G, Koleganova N, Ritz E, Müller A, Fedorova OV, Bagrov AY, et al. (2012). High salt intake causes adverse fetal programming—vascular effects beyond blood pressure. Nephrol Dial Transpl. 2012; 27(9): 3464-3476. DOI:10.1093/ndt/gfs027