The early development of the kidney and implications for future health

Journal of Developmental Origins of Health and Disease

Volumn 1, Issue 4, 2010, Pages 216-233

  Hoy, W E ^a   Ingelfinger, J R ^b   Hallan, S ^c   Hughson, M D ^d   Mott, S A ^a   Bertram, J F ^e  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b HARVARD MEDICAL SCHOOL   (United States)

^c NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^d UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^e MONASH UNIVERSITY   (Australia)

Author keywords

kidney development

Indexed keywords

EID: 84863897030     PISSN: 20401744     EISSN: 20401752     Source Type: Journal    
DOI: 10.1017/S204017441000022X     Document Type: Review

References (177)

1. Hoy, WE, Hughson, MD, Douglas-Denton, R, Bertram, JF, Amman, K. Nephron number, hypertension, renal disease and renal failure. J Am Soc Nephrol. 2005; 16, 2557–2564.
2. Moritz, KM, Cullen-McEwen, LA. Kidney development and fetal programming. Early Life origins of health and disease. Adv Exp Med Biol. 2006; 573, 130–143.
3. Bagby, SP. Maternal nutrition, low nephron number and hypertension in later life: pathways of nutritional programming. J Nutr. 2007; 137, 1066–1072.
4. Hoy, WE, Bertram, JF, Denton, RD, et-al. Nephron number, glomerular volume, renal disease and hypertension. Curr Opin Nephrol Hypertens. 2008; 17, 258–265.
5. Dotsch, J, Plank, C, Amann, K, Ingelfinger, J. The implications of fetal programming of glomerular number and renal function. J Mol Med. 2009; 87, 841–848.
6. Hinchliffe, SA, Sargent, PH, Howard, CV, Chan, YF, van Velzen, D. Human intrauterine renal growth expressed in absolute number of glomeruli assessed by the disector method and Cavalieri principle. Lab Invest. 1991; 64, 777–784.
7. Ekblom, P. Renal development. In The Kidney: Physiology and Pathophysiology (eds. Seldin DW, Giebisch G), 1992; pp. 475–501. Raven: New York.
8. Saxen, L. Organogenesis of the Kidney, 1987. Cambridge University Press: Cambridge.
9. Woolf, AS. Molecular bases of human kidney malformation. Pediatr nephrol. 1997; 22, 373–376.
10. Vize, PD, Woolf, AS, Bard, JBL. The Kidney: From Normal Development to Congenital Disease, 2003; Academic Press: London.
11. Madsen, KM, Tisher, CC. Structural-functional relationships along the distal nephron. Am J Physiol Renal Physiol. 1986; 250, F1–F15.
12. Hoy, WE, Douglas-Denton, RN, Hughson, M, et-al. A stereological study of glomerular number and volume: preliminary findings in a multiracial study of kidneys at autopsy. Kidney Int. 2003; 63, S31–S37.
13. Goldenberg, RL, Culhane, JF, Iams, JD, Romero, R. Epidemiology and causes of preterm birth. Lancet. 2008; 371, 75–84.
14. Laws, P, Abeywardana, S, Walker, J, Sullivan, E. Australia's Mothers and Babies. 2007. AIHW National Perinatal Statistics Unit: Sydney.
15. Rodriguez, MM, Gomez, AH, Abitbol, CL, et-al. Histomorphometric analysis of postnatal glomerulogenesis in extremely preterm infants. Pediatr Dev Pathol. 2004; 7, 17–25.
16. Gubhaju, L, Sutherland, MR, Yoder, BA, et-al. Is nephrogenesis affected by preterm birth? Studies in a non-human primate model. Am J Physiol Renal Physiol. 2009; 297, F1668–F1677.
17. Clark, AT, Bertram, JF. Molecular regulation of nephron endowment. Am J Physiol. 1999; 276(4 Pt 2), F485–F497.
18. Dressler, GR. The cellular basis of kidney development. Annu Rev Cell Dev Biol. 2006; 22, 509–529.
19. Moritz, KM, Wintour, EM, Black, MJ, Bertram, JF, Caruana, G. Factors influencing mammalian kidney development: implications for health in adult life. Adv Anat Embryol Cell Biol. 2008; 196, 1–78.
20. Kobayashi, A, Valerius, MT, Mugford, JW, et-al. Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell. 2008; 3, 169–181.
21. Sims-Lucas, S, Cullen-McEwen, L, Eswarakumar, VP, et-al. Deletion of Frs2alpha from the ureteric epithelium causes renal hypoplasia. Am J Physiol Renal Physiol. 2009; 297, F1208–F1219.
22. Stuart, RO, Bush, KT, Nigam, SK. Changes in gene expression patterns in the ureteric bud and metanephric mesenchyme in models of kidney development. Kidney Int. 2003; 64, 1997–2008.
23. Schwab, K, Patterson, LT, Aronow, BJ, et-al. A catalogue of gene expression in the developing kidney. Kidney Int. 2003; 64, 1588–1604.
24. Challen, G, Gardiner, B, Caruana, G, et-al. Temporal and spatial transcriptional programs in murine kidney development. Physiol Genomics. 2005; 23, 159–171.
25. Martinez, G, Georgas, K, Challen, GA, et-al. Definition and spatial annotation of the dynamic secretome during early kidney development. Dev Dyn. 2006; 235, 1709–1719.
26. Valerius, MT, Patterson, LT, Witte, DP, Potter, SS. Microarray analysis of novel cell lines representing two stages of metanephric mesenchyme differentiation. Mech Dev. 2002; 112, 219–232.
27. Takasato, M, Osafune, K, Matsumoto, Y, et-al. Identification of kidney mesenchymal genes by a combination of microarray analysis and Sall1-GFP knockin mice. Mech Dev. 2004; 121, 547–557.
28. Schmidt-Ott, KM, Yang, J, Chen, X, et-al. Novel regulators of kidney development from the tips of the ureteric bud. J Am Soc Nephrol. 2005; 16, 1993–2002.
29. Caruana, G, Young, RJ, Bertram, JF. Imaging the embryonic kidney. Nephron Exp Nephrol. 2006; 103, e62–e68.
30. Brunskill, EW, Aronow, BJ, Georgas, K, et-al. Atlas of gene expression in the developing kidney at microanatomic resolution. Dev Cell. 2008; 15, 781–791.
31. Moore, MW, Klein, RD, Farinas, I, et-al. Renal and neuronal abnormalities in mice lacking GDNF. Nature. 1996; 382, 76–79.
32. Pichel, JG, Shen, L, Sheng, HZ, et-al. Defects in enteric innervation and kidney development in mice lacking GDNF. Nature. 1996; 382, 73–76.
33. Suvanto, P, Hiltunen, JO, Arumae, U, et-al. Localization of glial cell line-derived neurotrophic factor (GDNF) mRNA in embryonic rat by in situ hybridization. Eur J Neurosci. 1996; 8, 816–822.
34. Cullen-McEwen, LA, Drago, J, Bertram, JF. Nephron endowment in glial cell line-derived neurotrophic factor (GDNF) heterozygous mice. Kidney Int. 2001; 60, 31–36.
35. Revest, JM, Spencer-Dene, B, Kerr, K, et-al. Fibroblast growth factor receptor 2-IIIb acts upstream of Shh and Fgf4 and is required for limb bud maintenance but not for the induction of Fgf8, Fgf10, Msx1, or Bmp4. Dev Biol. 2001; 231, 47–62.
36. Ohuchi, H, Hori, Y, Yamasaki, M, et-al. FGF10 acts as a major ligand for FGF receptor 2 IIIb in mouse multi-organ development. Biochem Biophys Res Commun. 2000; 277, 643–649.
37. Cacalano, G, Farinas, I, Wang, LC, et-al. GFRalpha1 is an essential receptor component for GDNF in the developing nervous system and kidney. Neuron. 1998; 21, 53–62.
38. McCright, B, Gao, X, Shen, L, et-al. Defects in development of the kidney, heart and eye vasculature in mice homozygous for a hypomorphic Notch2 mutation. Development. 2001; 128, 491–502.
39. Yu, J, Carroll, TJ, McMahon, AP. Sonic hedgehog regulates proliferation and differentiation of mesenchymal cells in the mouse metanephric kidney. Development. 2002; 129, 5301–5312.
40. Liu, J, Zhang, L, Wang, D, et-al. Congenital diaphragmatic hernia, kidney agenesis and cardiac defects associated with Slit3-deficiency in mice. Mech Dev. 2003; 120, 1059–1070.
41. Majumdar, A, Vainio, S, Kispert, A, McMahon, J, McMahon, AP. Wnt11 and Ret/Gdnf pathways cooperate in regulating ureteric branching during metanephric kidney development. Development. 2003; 130, 3175–3185.
42. Clarke, JC, Patel, SR, Raymond, RM Jr, et-al. Regulation of c-Ret in the developing kidney is responsive to Pax2 gene dosage. Hum Mol Genet. 2006; 15, 3420–3428.
43. Dziarmaga, A, Eccles, M, Goodyer, P. Suppression of ureteric bud apoptosis rescues nephron endowment and adult renal function in Pax2 mutant mice. J Am Soc Nephrol. 2006; 17, 1568–1575.
44. Sims-Lucas, S, Caruana, G, Dowling, J, Kett, MM, Bertram, JF. Augmented and accelerated nephrogenesis in TGF-beta2 heterozygous mutant mice. Pediatr Res. 2008; 63, 607–612.
45. Zhang, Z, Quinlan, J, Hoy, W, et-al. A common RET variant is associated with reduced newborn kidney size and function. J Am Soc Nephrol. 2008; 19, 2027–2034.
46. Quinlan, J, Lemire, M, Hudson, T, et-al. A common variant of the PAX2 gene is associated with reduced newborn kidney size. J Am Soc Nephrol. 2007; 18, 1915–1921.
47. Barker, DJ, Osmond, C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986; 1, 1077–1081.
48. Barker, DJ, Bull, AR, Osmond, C, Simmonds, SJ. Fetal and placental size and risk of hypertension in adult life. BMJ. 1990; 301, 259–262.
49. Brenner, BM, Chertow, GM. Congenital oligonephropathy and the etiology of adult hypertension and progressive renal injury. Am J Kidney Dis. 1994; 23, 171–175.
50. Singh, RR, Moritz, KM, Bertram, JF, Cullen-McEwen, LA. Effects of dexamethasone exposure on rat metanephric development: in vitro and in vivo studies. Am J Physiol Renal Physiol. 2007; 293, F548–F554.
51. Hoppe, CC, et-al. Effects of dietary protein restriction on nephron number in the mouse. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R1768–R1774.
52. Dickinson, H, et-al. Maternal dexamethasone treatment at midgestation reduces nephron number and alters renal gene expression in the fetal spiny mouse. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R453–R461.
53. Moritz, KM, Cullen-McEwen, LA. Kidney development and fetal programming. In Early Life Origins of Health and Disease (eds. Wintour EM and Owens JA), Advances in Experimental Medicine and Biolgoy, vol. 573, 2006; pp. 130–144. Springer Landes Bioscience: USA.
54. Nijland, MJ, Nathanielsz, PW. Developmental programming of the kidney. In Early Life Origins of Human Health and Disease (eds. JP Newnham and MG Ross), 2009; pp. 133–141. Karger: Basel.
55. Gray, SP, Kenna, K, Bertram, JF, et-al. Repeated ethanol exposure during late gestation decreases nephron endowment in fetal sheep. Am J Physiol Regul Integr Comp Physiol. 2008; 295, R568–R574.
56. Gray, SP, Denton, K, Bertram, JF, Moritz, KM. Acute prenatal alcohol exposure results in growth restriction, lower nephron endowment and elevated blood pressure in male rat offspring. Nephrology. 2008; 13(Suppl 3), A205.
57. Dodic, M, May, CN, Wintour, EM, Coghlan, JP. An early prenatal exposure to excess glucocorticoid leads to hypertensive offspring in sheep. Clin Sci (Lond). 1998; 94, 149–155.
58. Wintour, EM, Moritz, KM, Johnson, K, et-al. Reduced nephron number in adult sheep, hypertensive as a result of prenatal glucocorticoid treatment. J Physiol. 2003; 549, 929–935.
59. Woods, LL, Ingelfinger, JR, Nyengaard, JR, Rasch, R. Maternal protein restriction suppresses the newborn renin-angiotensin system and programs adult hypertension in rats. Pediatr Res. 2001; 49, 460–467.
60. Woods, LL, Weeks, DA, Rasch, R. Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int. 2004; 65, 1339–1348.
61. Zimanyi, MA, Bertram, JF, Black, MJ. Does a nephron deficit in rats predispose to salt-sensitive hypertension? Kidney Blood Press Res. 2004; 27, 239–247.
62. Hoppe, CC, Evans, RG, Moritz, KM, et-al. Combined prenatal and postnatal protein restriction influences adult kidney structure, function, and arterial pressure. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R462–R469.
63. Wlodek, ME, Mibus, A, Tan, A, et-al. Normal lactational environment restores nephron endowment and prevents hypertension after placental restriction in the rat. J Am Soc Nephrol. 2007; 18, 1688–1696.
64. Moritz, KM, Mazzuca, MQ, Siebel, AL, et-al. Uteroplacental insufficiency causes a nephron deficit, modest renal insufficiency but no hypertension with ageing in female rats. J Physiol. 2009; 587(Pt 11), 2635–2646.
65. Harrison, M, Langley-Evans, SC. Intergenerational programming of impaired nephrogenesis and hypertension in rats following maternal protein restriction during pregnancy. Br J Nutr. 2009; 101, 1020–1030.
66. National Kidney Foundation. K/DOQI clinical practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Kidney Disease Outcome Quality Initiative. Am J Kidney Dis. 2002; 39, S1–S246.
67. Fogo, AB. Mechanisms of progression of chronic kidney disease. Pediatr Nephrol. 2007; 22, 2011–2022.
68. Hallan, SI, Coresh, J, Astor, BC, et-al. International comparison of the relationship of chronic kidney disease prevalence and ESRD risk. J Am Soc Nephrol. 2006; 17, 2275–2284.
69. Coresh, J, Selvin, E, Stevens, LA, et-al. Prevalence of Chronic Kidney Disease in the United States. JAMA. 2007; 298, 2038–2047.
70. Zhang, L, Zhang, P, Wang, F, et-al. Prevalence and factors associated with CKD: a population study from Beijing. Am J Kidney Dis. 2008; 51, 373–384.
71. Hallan, SI, Astor, BC, Romundstad, S, et-al. Association of kidney function and albuminuria with cardiovascular mortality in older versus younger individuals; the HUNT II study. Arch Intern Med. 2007; 167, 2490–2496.
72. de Jong, PE, van der Velde, M, Gansevoort, RT, Zoccali, C. Screening for chronic kidney disease: where does Europe go? Clin J Am Soc Nephrol. 2008; 3, 616–623.
73. Taal, MW, Brenner, BM. Predicting initiation and progression of chronic kidney disease: developing renal risk scores. Kidney Int. 2006; 70, 1694–1705.
74. Hall, JE, Guyton, AC, Brands, MW. Pressure-volume regulation in hypertension. Kidney Int Suppl. 1996; 55, S35–S41.
75. Ritz, E. The role of the kidney in cardiovascular medicine. Eur J Intern Med. 2005; 16, 321–327.
76. Forsdahl, A. Living conditions in childhood and subsequent development of risk factors for arteriosclerotic heart disease. The cardiovascular survey in Finnmark 1974–75. J Epidemiol Community Health. 1978; 32, 34–37.
77. 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 Intern Med. 2000; 160, 1472–1476.
78. 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.
79. Fan, ZJ, Lackland, DT, Lipsitz, SR, Nicholas, JS. The association of low birthweight and chronic renal failure among Medicaid young adults with diabetes and/or hypertension. Public Health Rep. 2006; 121, 239–244.
80. Osmond, C, Barker, DJ, Winter, PD, Fall, CH, Simmonds, SJ. Early growth and death from cardiovascular disease in women. BMJ. 1993; 307, 1519–1524.
81. Huxley, R, Owen, CG, Whincup, PH, et-al. Is birth weight a risk factor for ischemic heart disease in later life? Am J Clin Nutr. 2007; 85, 1244–1250.
82. de Jong, PE, Curhan, GC. Screening, monitoring, and treatment of albuminuria: public health perspectives. J Am Soc Nephrol. 2006; 17, 2120–2126.
83. de Zeeuw, D, Parving, HH, Henning, RH. Microalbuminuria as an early marker for cardiovascular disease. J Am Soc Nephrol. 2006; 17, 2100–2105.
84. Hallan, SI, Ritz, E, Lydersen, S, et-al. Combining GFR and albuminuria to classify CKD improves prediction of ESRD. J Am Soc Nephrol. 2009; 20, 1069–1077.
85. Comper, WD, Hilliard, LM, Nikolic-Paterson, DJ, Russo, LM. Disease-dependent mechanisms of albuminuria. Am J Physiol Renal Physiol. 2008; 295, F1589–F1600.
86. Yudkin, JS, Martyn, CN, Phillips, DI, Gale, CR. Associations of micro-albuminuria with intra-uterine growth retardation. Nephron. 2001; 89, 309–314.
87. Painter, RC, Roseboom, TJ, van Montfrans, GA, et-al. Microalbuminuria in adults after prenatal exposure to the Dutch famine. J Am Soc Nephrol. 2005; 16, 189–194.
88. Fagerudd, J, Forsblom, C, Pettersson-Fernholm, K, et-al. Low birth weight does not increase the risk of nephropathy in Finnish type 1 diabetic patients. Nephrol Dial Transplant. 2006; 21, 2159–2165.
89. White, SL, Perkovic, V, Cass, A, et-al. Is low birth weight an antecedent of CKD in later life? A systematic review of observational studies. Am J Kidney Dis. 2009; 54, 248–261.
90. Li, S, Chen, SC, Shlipak, M, et-al. Low birth weight is associated with chronic kidney disease only in men. Kidney Int. 2007; 73, 637–642.
91. Law, CM, Shiell, AW. Is blood pressure inversely related to birth weight? The strength of evidence from a systematic review of the literature. J Hypertens. 1996; 14, 935–941.
92. Huxley, R, Neil, A, Collins, R. Unravelling the fetal origins hypothesis: is there really an inverse association between birthweight and subsequent blood pressure? Lancet. 2002; 360, 659–665.
93. Gamborg, M, Byberg, L, Rasmussen, F, et-al. Birth weight and systolic blood pressure in adolescence and adulthood: meta-regression analysis of sex- and age-specific results from 20 Nordic studies. Am J Epidemiol. 2007; 166, 634–645.
94. Langley-Evans, SC, Welham, SJM, Jackson, AA. Fetal exposure to maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci. 1999; 64, 965–974.
95. Lelièvre-Pégorier, M, Vilar, J, Ferrier, ML, et-al. Mild vitamin A deficiency leads to inborn nephron deficit in the rat. Kidney Int. 1998; 54, 1455–1462.
96. Merlet-Bénichou, C, Gilbert, T, Muffat-Joly, M, Lelièvre-Pégorier, M, Leroy, B. Intrauterine growth retardation leads to a permanent nephron deficit in the rat. Pediatr Nephrol. 1994; 8, 175–180.
97. Lewis, RM, Forhead, AJ, Petry, CJ, Ozanne, SE, Hales, CN. Long-term programming of blood pressure by maternal dietary iron restriction in the rat. Br J Nutr. 2002; 88, 283–290.
98. Hinchliffe, Vehaskari, MV, Aviles, DH, Manning, J. Prenatal programming of adult hypertension in the rat. Kidney Int. 2001; 59, 238–245.
99. Manning, J, Beutler, K, Knepper, MA, Vehaskari, VM. Upregulation of renal BSC1 and TSC in prenatally programmed hypertension. Am J Physiol Renal Physiol. 2002; 283, F202–F206.
100. Langley-Evans, SC, Sculley, DV. The association between birthweight and longevity in the rat is complex and modulated by maternal protein intake during fetal life. FEBS Lett 24. 2006; 580, 4150–4153; E-pub 30 Jun 2006.
101. Welham, SJ, Wade, A, Woolf, AS. Protein restriction in pregnancy is associated with increased apoptosis of mesenchymal cells at the start of rat metanephrogenesis. Kidney International. 2002; 61, 1231–1242.
102. Ortiz, LA, Quan, A, Weinberg, A, Baum, M. Effect of prenatal dexamethasone on rat renal development. Kidney Int. 2001; 59, 1663–1669.
103. Ortiz, LA, Quan, A, Zarzar, F, Weinberg, A, Baum, M. Prenatal dexamethasone programs hypertension and renal injury in the rat. Hypertension. 2003; 41, 328–334.
104. Dodic, M, Hantzis, V, Duncan, J, et-al. Programming effects of short prenatal exposure to cortisol. FASEB J. 2002; 16, 1017–1026.
105. Dodic, M, Peers, A, Moritz, K, Hantzis, V, Wintour, EM. No evidence for HPA reset in adult sheep with high blood pressure due to short prenatal exposure to dexamethasone. Am J Physiol Regul Integr Comp Physiol. 2002; 282, R343–R350.
106. Seckl, JR. Glucocorticoid programming of the fetus; adult phenotypes and molecular mechanisms. Mol Cell Endocrinol. 2001; 185, 61–71.
107. Doyle, LW, Ford, GW, Davis, NM, et-al. Antenatal corticosteroid therapy and blood pressure at 14 years of age in preterm children. Clin Sci (Lond). 2000; 98, 137–142.
108. Dessens, AB, Haas, HS, Koppe, JG. Twenty-year follow-up of antenatal corticosteroid treatment. Pediatrics. 2000; 105, E77.
109. Dalziel, SR, Walker, NK, Parag, V, et-al. Cardiovascular risk factors after antenatal exposure to betamethasone: 30-year follow-up of a randomized controlled trial. Lancet. 2005; 365, 1856–1862.
110. Finken, MJ, Keijzer-Veen, MG, Dekker, FW, et-al. Antenatal glucocorticoid treatment is not associated with long-term metabolic risks in individuals born before 32 weeks of gestation. Arch Dis Child Fetal Neonatal Ed. 2008; 93, F442–F447.
111. Wilson, JG, Warkany, J. Malformations in the genito-urinary tract induced by maternal vitamin A deficiency in the rat. Am J Anat. 1948; 83, 357–407.
112. Bhat, PV, Manolescu, DC. Role of vitamin A in determining nephron mass and possible relationship to hypertension. J Nutr. 2008; 138, 1407–1410.
113. Batourina, E, Gim, S, Bello, N, et-al. Vitamin A controls epithelial/mesenchymal interactions through Ret expression. Nat Genet. 2001; 27, 74–78.
114. Gilbert, T, Merlet-Benichou, C. Retinoids and nephron mass control. Pediatr Nephrol. 2000; 14, 1137–1144.
115. Merlet-Bénichou, C, Vilar, J, Lelièvre-Pégorier, M, Gilbert, T. Role of retinoids in renal development: pathophysiological implication. Curr Opin Nephrol Hypertens. 1999; 8, 39–43.
116. Mendelsohn, C, Lohnes, D, Décimo, D, et-al. Function of the retinoic acid receptors (RARs) during development. (II) Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development. 1994; 120, 2749–2771.
117. Makrakis, J, Zimanyi, MA, Black, MJ. Retinoic acid enhances nephron endowment in rats exposed to maternal protein restriction. Pediatr Nephrol. 2007; 22, 1861–1867.
118. Sutherland, MR, Gubahaju, L, Yoder, BA, Stahlman, MT, Black, MJ. The effects of postnatal retinoic administration on nephron endowment in the preterm baboon kidney. Paediatr Res. 2009; 65, 397–402.
119. Goodyer, P, Kurpad, A, Rekha, S, et-al. Effects of maternal vitamin A status on kidney development: a pilot study. Pediatr Nephrol. 2007; 22, 209–214.
120. Darlow, BA, Graham, PJ. Vitamin A supplementation to prevent mortality and short and long-term morbidity in very low birthweight infants. Cochrane Database Syst Rev. 2007; 17, CD000501 (Update of: Cochrane Database Syst Rev. 2002; (4): CD000501).
121. Xu, Q, Lucio-Cazana, J, Kitamura, M, et-al. Retinoids in nephrology: promises and pitfalls. Kidney Int. 2004; 66, 2119–2131.
122. Gambling, L, Dunford, S, Wallace, DI, et-al. Iron deficiency during pregnancy affects postnatal blood pressure in the rat. J Physiol. 2003; 552(Pt 2), 603–610.
123. Crowe, C, Dandekar, P, Fox, M, et-al. The effects of anaemia on heart, placenta and body weight, and blood pressure in fetal and neonatal rats. J Physiol. 1995; 488(Pt 2), 515–519.
124. Singla, PN, Tyagi, M, Kumar, A, Dash, D, Shankar, R. Fetal growth in maternal anaemia. J Trop Pediatr. 1997; 43, 89–92.
125. Lieberman, E, Ryan, KJ, Monson, RR, Schoenbaum, SC. Association of maternal hematocrit with premature labor. Am J Obstet Gynecol. 1988; 159, 107–114.
126. Scholl, TO, Hediger, ML, Fischer, RL, Shearer, JW. Anemia vs iron deficiency: increased risk of preterm delivery in a prospective study. Am J Clin Nutr. 1992; 55, 985–988.
127. Lu, ZM, Goldenberg, RL, Cliver, SP, Cutter, G, Blankson, M. The relationship between maternal hematocrit and pregnancy outcome. Obstet Gynecol. 1991; 77, 190–194.
128. Tamura, T, Goldenberg, RL, Johnston, KE, Cliver, SP, Hickey, CA. Serum ferritin: a predictor of early spontaneous preterm delivery. Obstet Gynecol. 1996; 87, 360–365.
129. Knottnerus, JA, Delgado, LR, Knipschild, PG, Essed, GG, Smits, F. Haematologic parameters and pregnancy outcome. A prospective cohort study in the third trimester. J Clin Epidemiol. 1990; 43, 461–466.
130. Cogswell, ME, Parvanta, I, Ickes, L, Yip, R, Brittenham, GM. Iron supplementation during pregnancy, anemia, and birth weight: a randomized controlled trial. Am J Clin Nutr. 2003; 78, 773–781.
131. Belfort, MB, Rifas-Shiman, SL, Rich-Edwards, JW, et-al. Maternal iron intake and iron status during pregnancy and child blood pressure at age 3 years. Int J Epidemiol. 2008; 37, 301–308.
132. Whincup, P, Cook, D, Papacosta, O, Walker, M, Perry, I. Maternal factors and development of cardiovascular risk: evidence from a study of blood pressure in children. J Hum Hypertens. 1994; 8, 337–343.
133. Siewert-Delle, A, Ljungman, S. The impact of birth weight and gestational age on blood pressure in adult life: a population-based study of 49-year-old men. Am J Hypertens. 1998; 11, 946–953.
134. Nuyt, AM, Alexander, BT. Developmental programming and hypertension. Curr Opin Nephrol Hypertens. 2009; 18, 144–152.
135. Usher, R, McLean, F. Intrauterine growth of live-born Caucasian infants at sea level: standards obtained from measurements in 7 dimensions of infants born between 25 and 44 weeks of gestation. J Pediatr. 1969; 74, 901–910.
136. Liew, G, Wang, JJ, Mitchell, P. Which is the better marker for susceptibility to disease later in life: low birthweight or prematurity? Arch Dis Child. 2008; 93, 450.
137. Rakow, A, Johansson, S, Legnevall, L, et-al. Renal volume and function in school-age children born preterm or small for gestational age. Pediatr Nephrol. 2008; 23, 1309–1315; E-pub 6 May 2008.
138. Kent, AL, Jyoti, R, Robertson, C, et-al. Does extreme prematurity affect kidney volume at term corrected age? J Matern Fetal Neonatal Med. 2009; 22, 435–438.
139. Bacchetta, J, Harambat, J, Dubourg, L, et-al. Both extrauterine and intrauterine growth restriction impair renal function in children born very preterm. Kidney Int. 2009; 76, 445–452.
140. Sutherland, M, Gubhaju, L, Stamp, L, et-al. Preterm birth is associated with accelerated glomerular maturation and the formation of abnormal glomeruli. Nephrol. 2009; 14 (Suppl 1), A14, Abstract 052.
141. Hodgin, JB, Rasoulpour, M, Markowitz, GS, D’Agati, VD. Very low birth weight is a risk factor for secondary focal segmental glomerulosclerosis. Clin J Am Soc Nephrol. 2009; 4, 71–76; E-pub 19 November 2008.
142. Abitbol, CL, Bauer, CR, Montane, B, et-al. Long term follow up of extremely low birthweight infants with neonatal renal failure. Pediatr Nephrol. 2003; 18, 887–893.
143. Al Salmi, I, Hoy, WE, Healy, H, et-al. Birthweight and chronic kidney disease: a case-control study in an Australian population. Am J Kid Dis. 2008; 52, 1070–1078.
144. Lackland, DT, Barker, DJ. Birthweight: a predictive medicine consideration for the disparities in CKD. Am J Kid Dis. 2009; 53, 191–193.
145. Hoy, WE, Mathews, JD, Pugsley, DJ, et-al. The multidimensional nature of renal disease: rates and associations of albuminuria in an Australian Aboriginal community. Kidney Int. 1998; 54, 1296–1304.
146. Nenov, VD, Taal, MW, Sakharova, OV, Brenner, BM. Multi-hit nature of chronic renal disease. Curr Opin Nephrol Hypertens. 2000; 9, 85–97.
147. Hoy, WE, Kile, E, Rees, M, Mathews, JD. A new dimension to the Barker hypothesis: low birth weight and susceptibility to renal disease: findings in an Australian Aboriginal community. Kidney Int. 1999; 56, 1072–1076.
148. Bruce, MA, Beech, BM, Sims, M, et-al. Social environmental stressors, psychological factors and kidney disease. J Investig Med. 2009; 57, 583–589.
149. Hoy, WE, Nichol, JL. Birthweight and natural death in a remote Aboriginal community. Med J Aust. 2010; 192, 14–19.
150. Hoy, WE, Kile, E, Rees, M, Mathews, JD. Low birth weight and renal disease in Australian Aborigines. The Lancet. 1998; 352, 1826–1827.
151. Singh, GR, Hoy, WE. Kidney volume, blood pressure, and albuminuria: findings in an Australian aboriginal community. Am J Kid Disease. 2004; 43, 254–259.
152. Hoy, WE, Kondalsamy-Chennakesavan, S, et al. Final Report to Australian Kidney Foundation and the Office of Aboriginal and Torres Strait Islander Health (OATSIH) on the NT Aboriginal Chronic Disease Outreach Program, 2004. Retrieved 31 October 2004 from http://www.healthinfonet.ecu.edu.au.
153. Hoy, WE, Hughson, MD, Zimanyi, M, et-al. Distribution of Volumes of Individual Glomeruli in Kidneys at Autopsy: Association with Age, Nephron Number, Birthweight and Body Mass Index. Am J Nephrol. 2009. Accepted December 2009.
154. Samuel, T, Hoy, WE, Douglas-Denton, R, Hughson, MD, Bertram, JF. Determinants of glomerular volumes in different cortical zones of the human kidney. J Am Soc Nephrol. 2005; 16, 3102–3109.
155. Zimanyi, MA, Hoy, WE, Douglas-Denton, RN, et-al. Nephron number and individual glomerular volumes in male Caucasian and African American subjects. Nephrol Dial Transplant. 2009; 24, 2428–2433.
156. McNamara, BJ, Diouf, B, Hughson, MD, Hoy, WE, Bertram, JF. Associations between age, body size and nephron number with individual glomerular volumes in urban West African males. Nephrol Dial Transplant. 2009; 24, 1500–1506.
157. Hoy, WE, Zimanyi, MA, Samuel, T, et-al. Distribution of volumes of different glomeruli within individuals: findings in kidneys at coronial autopsy. Australian and New Zealand Society of Nephrology 45th Annual Scientific Meeting, 7–9 September 2009, Hobart, Australia. Nephrology. 2009; 14(Suppl 1), A15(056).
158. Fogo, A, Ichikawa, I. Evidence for a pathogenetic link between glomerular hypertrophy and sclerosis. Am J Kidney Dis. 1991; 17, 666–669.
159. Brenner, BM, Lawler, EV, Mackenzie, HS. The hyperfiltration theory: a paradigm shift in nephrology. Kidney Int. 1996; 49, 1774–1777.
160. Hughson, M, Farris, AB 3rd, Douglas-Denton, R, et-al. Glomerular number and size in autopsy kidneys: the relationship to birthweight. Kidney Int. 2003; 63, 2113–2122.
161. Hoy, WE, Hughson, MD, Singh, GR, et-al. Reduced nephron number and glomerulomegaly in Australian Aborigines: a group at high risk for renal disease and hypertension. Kidney Int. 2006; 70, 4–110.
162. McNamara, BJ, Diouf, B, Douglas-Denton, R, Hughson, MD, Hoy, WE, Bertram, JF. A comparison of nephron number, glomerular volume and kidney weight in Senegalese Africans and African Americans. Nephrol Dial Transplant. 2010; E-pub ahead of print, 11 February 2010.
163. Keller, G, Zimmer, G, Mall, G, et-al. Nephron number in patients with primary hypertension. N Engl J Med. 2003; 348, 101–108.
164. Ingelfinger, J. Is microanatomy destiny. New Engl J Med. 2003; 348, 99–1010.
165. Nyengaard, JR, Bendtsen, TF. Glomerular number and size in relation to age, kidney weight and body surface area in normal man. Anat Record. 1992; 232, 1940201.
166. Howard, D, Davis, J, Pugsley, JD, Seymour, A, Hoy, WE. Morphologic correlates of renal disease in a high risk Australian Aboriginal community Aust NZ Soc Nephrol, 32nd Annual Meeting, Perth, March 5–8, 1996. Kidney Int. 1997; 51, p. 1318.
167. Bertram, JF, Young, RJ, Kincaid-Smith, P, Seymour, AE, Hoy, WE. Glomerulomegaly in Australian Aborigines. Nephrology. 1998; 4, S46–S53.
168. Young, RJ, Hoy, WE, Kincaid Smith, P, Seymour, AE, Bertram, JF. Glomerular size and glomerulosclerosis in Australian Aborigines. Am J Kidney Dis. 2000; 36, 481–489.
169. Hoy, WE, Samuel, T, Hughson, MD, etal.; and Members of the National Aboriginal Renal Biopsy Study Group. Kidney biopsy findings from Aboriginal people in the Northern Territory, Central Australia and Western Australia. Nephrology. 2005; 10(Suppl pA380), PS8.
170. Kincaid Smith, P, Hoy, WE, Hughson, MD, etal.; and Members of the National Aboriginal Renal Biopsy Study Group. High rates of segmental glomerular injury in Aboriginal kidney biopsies. 41st Annual Scientific Meeting of the ANZSN, Wellington, Sept 2005. Nephrology. 2005; 10(Suppl), PS21 pA384.
171. Hoy, WE, on behalf of the Collaborative Study Group for Nationwide Indigenous Australian Renal Biopsies. Clinical and Morphologic Features in a Nationwide Series of Renal Biopsies of Indigenous Australians. Abstract presented at: The American Society of Nephrology Renal Week, Philadelphia, PA, November, 2008, SA-PO2461. J Am Soc Nephrol (Abstracts Issue 200819), 662A, October 2008.
172. Douglas-Denton, RN, Hoy, WE, Bertram, JE, et al., on behalf of the Indigenous Australian Renal Biopsy Study Group. Demographic Features of Indigenous Australians in a Nationwide Review of Renal Biopsies. 44th Annual Scientific Meeting of the Australian and New Zealand Society of Nephrology, Newcastle, Sept 2008. Poster.
173. Mott, SA, Hoy, WE, Bertram, JE, et al., on behalf of the Indigenous Australian Renal Biopsy Study Group. Clinical Features of Indigenous Australians in a Nationwide Review of Renal Biopsies. 44th Annual Scientific Meeting of the Australian and New Zealand Society of Nephrology, Newcastle, Sept 2008. Poster.
174. Kincaid Smith, P, Hoy, WE, Hughson, MD, et al. Kidney biopsy findings from Aboriginal people in Remote Areas in Australia: Focal and Segmental Glomeruloscerosis, insulin resistance and Type 2 Diabetes. Abstract presented at: World Congress of Nephrology, Rio De Janeiro, Brazil, 21–25th April 2007.
175. Hoy, WE, on behalf of the Collaborative Study Group for Nationwide Indigenous Australian Renal Biopsies. Comparison of Findings in Diabetics and Nondiabetics in a Nationwide Study of Renal Biopsies in Indigenous Australians. J Am Soc Nephrol. 19 Abstracts Issue, October 2008.
176. Hoy, WE, Kondalsamy Chennakesavan, S, Shaw, J, et-al. Estimating the excess risk for hypertension, renal disease and diabetes among of Aboriginal in remote communities in the Northern Territory. Aust NZ J Public Health. 2007; 31, 177–183.
177. Wang, Z, Hoy, WE. Albuminuria and risk of developing diabetes in Aboriginal Australians. Int J Epidemiol. 2006; 35, 1331–1335.