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The relationship between maternal obesity and diabetes during pregnancy on offspring kidney structure and function in humans: a systematic review

Published online by Cambridge University Press:  09 November 2018

Y. Q. Lee ,
C. E. Collins ,
A. Gordon ,
K. M. Rae  and
K. G. Pringle
Y. Q. Lee
Affiliation:
School of Biomedical Sciences and Pharmacy, Faculty of Health and Medicine, University of Newcastle, Newcastle, NSW, Australia Priority Research Centre for Reproductive Sciences, University of Newcastle, Newcastle, NSW, Australia
C. E. Collins
Affiliation:
School of Health Sciences, Faculty of Health and Medicine, University of Newcastle, Newcastle, NSW, Australia Priority Research Centre in Physical Activity and Nutrition, University of Newcastle, Newcastle, NSW, Australia
A. Gordon
Affiliation:
Charles Perkins Centre, University of Sydney, Sydney, NSW, Australia
K. M. Rae
Affiliation:
Priority Research Centre for Reproductive Sciences, University of Newcastle, Newcastle, NSW, Australia Gomeroi gaaynggal Centre, Faculty of Health and Medicine, University of Newcastle, Tamworth, NSW, Australia Department of Rural Health, School of Medicine and Public Health, Faculty of Health and Medicine, University of Newcastle, Tamworth, NSW, Australia Priority Research Centre for Generational Health and Ageing, University of Newcastle, Newcastle, NSW, Australia
K. G. Pringle*
Affiliation:
School of Biomedical Sciences and Pharmacy, Faculty of Health and Medicine, University of Newcastle, Newcastle, NSW, Australia Priority Research Centre for Reproductive Sciences, University of Newcastle, Newcastle, NSW, Australia Gomeroi gaaynggal Centre, Faculty of Health and Medicine, University of Newcastle, Tamworth, NSW, Australia
*
Address for correspondence: Dr. K. G. Pringle, Hunter Medical Research Institute, Lot 1 Kookaburra Circuit, New Lambton Heights, NSW 2305, Australia. E-mail: kirsty.pringle@newcastle.edu.au
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Abstract

Evidence from animal models indicates that exposure to an obesogenic or hyperglycemic intrauterine environment adversely impacts offspring kidney development and renal function. However, evidence from human studies has not been evaluated systematically. Therefore, the aim of this systematic review was to synthesize current research in humans that has examined the relationship between gestational obesity and/or diabetes and offspring kidney structure and function. Systematic electronic database searches were conducted of five relevant databases (CINAHL, Cochrane, EMBASE, MEDLINE and Scopus). Preferred Reporting Items for Systematic Reviews and Meta-analysis guidelines were followed, and articles screened by two independent reviewers generated nine eligible papers for inclusion. Six studies were assessed as being of ‘neutral’ quality, two of ‘negative’ and one ‘positive’ quality. Observational studies suggest that offspring exposed to a hyperglycemic intrauterine environment are more likely to display markers of renal dysfunction and are at higher risk of end-stage renal disease. There was limited and inconsistent evidence for a link between exposure to an obesogenic intrauterine environment and offspring renal outcomes. Offspring renal outcome measures across studies were diverse, with a large variation in offspring age at follow-up, limiting comparability across studies. The collective current body of evidence suggests that intrauterine exposure to maternal obesity and/or diabetes adversely impacts renal programming in offspring, with an increased risk of kidney disease in adulthood. Further high-quality, longitudinal, prospective cohort studies that measure indicators of offspring renal development and function, including fetal kidney volume and albuminuria, at standardized follow-up time points, are warranted.

Keywords

diabeteskidney diseaseobesitypregnancy
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 10 , Issue 4 , August 2019 , pp. 406 - 419
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

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References

Barker, DJP. Developmental origins of chronic disease. Public Health. 2012; 126, 185–189.CrossRefGoogle ScholarPubMed
Barker, DJP. Intrauterine programming of adult disease. Mol Med Today. 1995; 1, 418–423.CrossRefGoogle ScholarPubMed
Barker, DJP. Developmental origins of adult health and disease. J Epidemiol Community Health. 2004; 58, 114–115.CrossRefGoogle ScholarPubMed
Langley-Evans, SC. Developmental programming of health and disease. Proc Nutr Soc. 2006; 65, 97–105.CrossRefGoogle ScholarPubMed
Couser, WG, Remuzzi, G, Mendis, S, Tonelli, M. The contribution of chronic kidney disease to the global burden of major noncommunicable diseases. Kidney Int. 2011; 80, 1258–1270.CrossRefGoogle ScholarPubMed
Ingelfinger, JR, Kalantar-Zadeh, K, Schaefer, F. Averting the legacy of kidney disease: focus on childhood. Future Sci OA. 2016; 2, Fso112.CrossRefGoogle ScholarPubMed
Bertram, JF, Douglas-Denton, RN, Diouf, B, Hughson, MD, Hoy, WE. Human nephron number: implications for health and disease. Pediatr Nephrol. 2011; 26, 1529.CrossRefGoogle ScholarPubMed
Dressler, GR. The cellular basis of kidney development. Annu Rev Cell Dev Biol. 2006; 22, 509–529.CrossRefGoogle ScholarPubMed
Brenner, BM, Garcia, DL, Anderson, S. Glomeruli and blood pressure. Less of one, more the other? Am J Hypertens. 1988; 1, 335–347.CrossRefGoogle ScholarPubMed
Helal, I, Fick-Brosnahan, GM, Reed-Gitomer, B, Schrier, RW. Glomerular hyperfiltration: definitions, mechanisms and clinical implications. Nat Rev Nephrol. 2012; 8, 293–300.CrossRefGoogle ScholarPubMed
Dorey, ES, Pantaleon, M, Weir, KA, Moritz, KM. Adverse prenatal environment and kidney development: implications for programing of adult disease. Reproduction (Cambridge, England). 2014; 147, R189–198.CrossRefGoogle ScholarPubMed
Luyckx, VA, Perico, N, Somaschini, M, et al. A developmental approach to the prevention of hypertension and kidney disease: a report from the Low Birth Weight and Nephron Number Working Group. Lancet (London, England). 2017; 390, 424–428.CrossRefGoogle ScholarPubMed
Tran, S, Chen, YW, Chenier, I, et al. Maternal diabetes modulates renal morphogenesis in offspring. J Am Soc Nephrol. 2008; 19, 943–952.CrossRefGoogle ScholarPubMed
Yan, J, Li, X, Su, R, Zhang, K, Yang, H. Long-term effects of maternal diabetes on blood pressure and renal function in rat male offspring. PLoS One. 2014; 9, e88269.CrossRefGoogle ScholarPubMed
Chen, YW, Chenier, I, Tran, S, et al. Maternal diabetes programs hypertension and kidney injury in offspring. Pediatr Nephrol (Berlin, Germany). 2010; 25, 1319–1329.CrossRefGoogle ScholarPubMed
Khan, IY, Taylor, PD, Dekou, V, et al. Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension (Dallas, TX: 1979). 2003; 41, 168–175.CrossRefGoogle ScholarPubMed
Taylor, PD, Khan, IY, Lakasing, L, et al. Uterine artery function in pregnant rats fed a diet supplemented with animal lard. Exp Physiol. 2003; 88, 389–398.CrossRefGoogle ScholarPubMed
Wood-Bradley, RJ, Barrand, S, Giot, A, Armitage, JA. Understanding the role of maternal diet on kidney development; an opportunity to improve cardiovascular and renal health for future generations. Nutrients. 2015; 7, 1881–1905.CrossRefGoogle ScholarPubMed
Altunkaynak, ME, Özbek, E, Altunkaynak, BZ, et al. The effects of high-fat diet on the renal structure and morphometric parametric of kidneys in rats. J Anat. 2008; 212, 845–852.CrossRefGoogle ScholarPubMed
Armitage, JA, Lakasing, L, Taylor, PD, et al. Developmental programming of aortic and renal structure in offspring of rats fed fat-rich diets in pregnancy. J Physiol. 2005; 565, 171–184.CrossRefGoogle ScholarPubMed
Glastras, SJ, Chen, H, McGrath, RT, et al. Effect of GLP-1 receptor activation on offspring kidney health in a rat model of maternal obesity. Sci Rep. 2016; 6, 23525.CrossRefGoogle Scholar
Blumfield, ML, Hure, AJ, MacDonald-Wicks, LK, et al. Dietary balance during pregnancy is associated with fetal adiposity and fat distribution. Am J Clin Nutr. 2012; 96, 1032–1041.CrossRefGoogle ScholarPubMed
Blumfield, ML, Nowson, C, Hure, AJ, et al. Lower protein-to-carbohydrate ratio in maternal diet is associated with higher childhood systolic blood pressure up to age four years. Nutrients. 2015; 7, 3078–3093.CrossRefGoogle ScholarPubMed
Centre for Reviews and Dissemination. Systematic Reviews: CRD’s Guidance for Undertaking Reviews in Health Care. University of York: New York, NY, USA, 2008.Google Scholar
Moher, D, Liberati, A, Tetzlaff, J, Altman, DG, The, PG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009; 6, e1000097.CrossRefGoogle ScholarPubMed
Lee, YQ, Collins, CE, Gordon, A, Rae, KM, Pringle, KG. The relationship between maternal nutrition during pregnancy and offspring kidney structure and function in humans: a systematic review. Nutrients. 2018; 10, E241. CrossRefGoogle ScholarPubMed
American Dietetic Association. ADA Quality Criteria Checklist: Primary Research. Chicago, IL, 2008.Google Scholar
Nelson, RG, Morgenstern, H, Bennett, PH. Intrauterine diabetes exposure and the risk of renal disease in diabetic Pima Indians. Diabetes. 1998; 47, 1489–1493.CrossRefGoogle ScholarPubMed
Pavkov, ME, Hanson, RL, Knowler, WC, et al. Effect of intrauterine diabetes exposure on the incidence of end-stage renal disease in young adults with type 2 diabetes. Diabetes Care. 2010; 33, 2396–2398.CrossRefGoogle ScholarPubMed
Hsu, CW, Yamamoto, KT, Henry, RK, De Roos, AJ, Flynn, JT. Prenatal risk factors for childhood CKD. J Am Soc Nephrol. 2014; 25, 2105–2111.CrossRefGoogle ScholarPubMed
Bos, AF, Aalders, AL, van Doormaal, JJ, Martijn, A, Okken, A. Kidney size in infants of tightly controlled insulin-dependent diabetic mothers. J Clin Ultrasound. 1994; 22, 443–446.CrossRefGoogle ScholarPubMed
Verburg, BO, Geelhoed, JJ, Steegers, EA, et al. Fetal kidney volume and its association with growth and blood flow in fetal life: The Generation R Study. Kidney Int. 2007; 72, 754–761.CrossRefGoogle ScholarPubMed
Dyck, RF, Bingham, WT, Lim, H, Jiang, Y, Osgood, ND. Decreased urine albumin:creatinine ratios in infants of diabetic mothers: does exposure to diabetic pregnancies alter fetal renal development? J Dev Orig Health Dis. 2011; 2, 265–271.CrossRefGoogle ScholarPubMed
Abi Khalil, C, Travert, F, Fetita, S, et al. Fetal exposure to maternal type 1 diabetes is associated with renal dysfunction at adult age. Diabetes. 2010; 59, 2631–2636.CrossRefGoogle ScholarPubMed
Cappuccini, B, Torlone, E, Ferri, C, et al. Renal echo-3D and microalbuminuria in children of diabetic mothers: a preliminary study. J Dev Orig Health Dis. 2013; 4, 285–289.CrossRefGoogle ScholarPubMed
Neves, HM, Sgarbosa, F, Calderon, IM, et al. Does hyperglycemia in pregnancy change fetal kidney growth? A longitudinal prospective study. Revista Brasileira de Ginecologia e Obstetrícia. 2013; 35, 442–446.CrossRefGoogle ScholarPubMed
Ma, RC, Chan, JC, Tam, WH, Hanson, MA, Gluckman, PD. Gestational diabetes, maternal obesity, and the NCD burden. Clin Obstet Gynecol. 2013; 56, 633–641.CrossRefGoogle ScholarPubMed
Lozano, R, Naghavi, M, Foreman, K, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet (London, England). 2012; 380, 2095–2128.CrossRefGoogle ScholarPubMed
Mills, KT, Xu, Y, Zhang, W, et al. A systematic analysis of worldwide population-based data on the global burden of chronic kidney disease in 2010. Kidney Int. 2015; 88, 950–957.CrossRefGoogle ScholarPubMed
GBD 2013 Mortality and Causes of Death Collaborators. Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2014; 385, 117–171.Google Scholar
Nicholas, SB, Kalantar-Zadeh, K, Norris, KC. Racial disparities in kidney disease outcomes. Semin Nephrol. 2013; 33, 409–415.CrossRefGoogle ScholarPubMed
Dickinson, H, Moss, TJ, Gatford, KL, et al. A review of fundamental principles for animal models of DOHaD research: an Australian perspective. J Dev Orig Health Dis. 2016; 7, 449–472.CrossRefGoogle Scholar
Kampmann, U, Madsen, LR, Skajaa, GO, et al. Gestational diabetes: a clinical update. World J Diabetes. 2015; 6, 1065–1072.CrossRefGoogle ScholarPubMed
Mitanchez, D. Foetal and neonatal complications in gestational diabetes: perinatal mortality, congenital malformations, macrosomia, shoulder dystocia, birth injuries, neonatal complications. Diabetes Metab. 2010; 36, 617–627.CrossRefGoogle ScholarPubMed
Mitanchez, D, Yzydorczyk, C, Siddeek, B, et al. The offspring of the diabetic mother—short- and long-term implications. Best Pract Res Clin Obstet Gynaecol. 2015; 29, 256–269.CrossRefGoogle ScholarPubMed
Luyckx, VA, Brenner, BM. Birth weight, malnutrition and kidney-associated outcomes—a global concern. Nat Rev Nephrol. 2015; 11, 135–149.CrossRefGoogle ScholarPubMed
Lackland, DT, Bendall, HE, Osmond, C, Egan, BM, Barker, DJ. Low birth weights contribute to high rates of early-onset chronic renal failure in the Southeastern United States. Arch Internal Med. 2000; 160, 1472–1476.CrossRefGoogle ScholarPubMed
Vikse, BE, Irgens, LM, Leivestad, T, Hallan, S, Iversen, BM. Low birth weight increases risk for end-stage renal disease. J Am Soc Nephrol. 2008; 19, 151–157.CrossRefGoogle ScholarPubMed
Amri, K, Freund, N, Vilar, J, Merlet-Benichou, C, Lelievre-Pegorier, M. Adverse effects of hyperglycemia on kidney development in rats: in vivo and in vitro studies. Diabetes. 1999; 48, 2240–2245.CrossRefGoogle ScholarPubMed
Amri, K, Freund, N, Duong Van Huyen, JP, Merlet-Benichou, C, Lelievre-Pegorier, M. Altered nephrogenesis due to maternal diabetes is associated with increased expression of IGF-II/mannose-6-phosphate receptor in the fetal kidney. Diabetes. 2001; 50, 1069–1075.CrossRefGoogle ScholarPubMed
Jones, SE, Bilous, RW, Flyvbjerg, A, Marshall, SM. Intra-uterine environment influences glomerular number and the acute renal adaptation to experimental diabetes. Diabetologia. 2001; 44, 721–728.CrossRefGoogle ScholarPubMed
Fetita, LS, Sobngwi, E, Serradas, P, Calvo, F, Gautier, JF. Consequences of fetal exposure to maternal diabetes in offspring. J Clin Endocrinol Metab. 2006; 91, 3718–3724.CrossRefGoogle ScholarPubMed
Ben-Haroush, A, Chen, R, Hadar, E, Hod, M, Yogev, Y. Accuracy of a single fetal weight estimation at 29-34 weeks in diabetic pregnancies: can it predict large-for-gestational-age infants at term? Am J Obstet Gynecol. 2007; 197, 497.e491–496.CrossRefGoogle ScholarPubMed
Hill, DJ, Petrik, J, Arany, E. Growth factors and the regulation of fetal growth. Diabetes Care. 1998; 21(Suppl 2), B60–69.Google ScholarPubMed
Nyengaard, JR, Bendtsen, TF. Glomerular number and size in relation to age, kidney weight, and body surface in normal man. Anat Rec. 1992; 232, 194–201.CrossRefGoogle ScholarPubMed
Abitbol, CL, Ingelfinger, JR. Nephron mass and cardiovascular and renal disease risks. Semin Nephrol. 2009; 29, 445–454.CrossRefGoogle ScholarPubMed
Keller, G, Zimmer, G, Mall, G, Ritz, E, Amann, K. Nephron number in patients with primary hypertension. N Engl J Med. 2003; 348, 101–108.CrossRefGoogle ScholarPubMed
Singh, GR, Hoy, WE. Kidney volume, blood pressure, and albuminuria: findings in an Australian aboriginal community. Am J Kidney Dis. 2004; 43, 254–259.CrossRefGoogle Scholar
Singh, GR, White, AV, Hoy, WE. Renal ultrasound findings in an Australian Aboriginal population with high rates of renal disease. Nephrology. 2005; 10, 358–361.CrossRefGoogle Scholar
Widjaja, E, Oxtoby, JW, Hale, TL, et al. Ultrasound measured renal length versus low dose CT volume in predicting single kidney glomerular filtration rate. Br J Radiol. 2004; 77, 759–764.CrossRefGoogle ScholarPubMed
Herts, BR, Sharma, N, Lieber, M, et al. Estimating glomerular filtration rate in kidney donors: a model constructed with renal volume measurements from donor CT scans. Radiology. 2009; 252, 109–116.CrossRefGoogle ScholarPubMed
Kariyanna, SS, Light, RP, Agarwal, R. A longitudinal study of kidney structure and function in adults. Nephrol Dial Transplant. 2010; 25, 1120–1126.CrossRefGoogle ScholarPubMed
Christiansen, JS, Gammelgaard, J, Frandsen, M, Parving, HH. Increased kidney size, glomerular filtration rate and renal plasma flow in short-term insulin-dependent diabetics. Diabetologia. 1981; 20, 451–456.CrossRefGoogle ScholarPubMed
Wirta, O, Pasternack, A, Laippala, P, Turjanmaa, V. Glomerular filtration rate and kidney size after six years disease duration in non-insulin-dependent diabetic subjects. Clin Nephrol. 1996; 45, 10–17.Google ScholarPubMed
Gragnoli, G, Signorini, AM, Tanganelli, I, et al. Prevalence of glomerular hyperfiltration and nephromegaly in normo- and microalbuminuric type 2 diabetic patients. Nephron. 1993; 65, 206–211.CrossRefGoogle ScholarPubMed
Rigalleau, V, Garcia, M, Lasseur, C, et al. Large kidneys predict poor renal outcome in subjects with diabetes and chronic kidney disease. BMC Nephrol. 2010; 11, 3–3.CrossRefGoogle ScholarPubMed
Thangaratinam, S, Rogozinska, E, Jolly, K, et al. Effects of interventions in pregnancy on maternal weight and obstetric outcomes: meta-analysis of randomised evidence. BMJ (Clin Res). 2012; 344, e2088.Google ScholarPubMed
Reynolds, RM, Allan, KM, Raja, EA, et al. Maternal obesity during pregnancy and premature mortality from cardiovascular event in adult offspring: follow-up of 1 323 275 person years. BMJ (Clin Res). 2013; 347, f4539.Google Scholar
Tarantal, AF, Berglund, L. Obesity and lifespan health—importance of the fetal environment. Nutrients. 2014; 6, 1725–1736.CrossRefGoogle ScholarPubMed
Laitinen, J, Jaaskelainen, A, Hartikainen, AL, et al. Maternal weight gain during the first half of pregnancy and offspring obesity at 16 years: a prospective cohort study. BJOG: Int J Obstet Gynaecol. 2012; 119, 716–723.CrossRefGoogle ScholarPubMed
Guo, SS, Wu, W, Chumlea, WC, Roche, AF. Predicting overweight and obesity in adulthood from body mass index values in childhood and adolescence. Am J Clin Nutr. 2002; 76, 653–658.CrossRefGoogle ScholarPubMed
Flynn, ER, Alexander, BT, Lee, J, Hutchens, ZM Jr., Maric-Bilkan, C. High-fat/fructose feeding during prenatal and postnatal development in female rats increases susceptibility to renal and metabolic injury later in life. Am J Physiol. 2013; 304, R278–285.Google ScholarPubMed
Jackson, CM, Alexander, BT, Roach, L, et al. Exposure to maternal overnutrition and a high-fat diet during early postnatal development increases susceptibility to renal and metabolic injury later in life. Am J Physiol Renal Physiol. 2012; 302, F774–783.CrossRefGoogle Scholar