Advertisement

Reproductive Sciences

, Volume 18, Issue 4, pp 322–333 | Cite as

Preterm Birth and the Kidney: Implications for Long-Term Renal Health

  • Lina Gubhaju
  • Megan R. Sutherland
  • M. Jane BlackEmail author
Review

Abstract

Although the majority of preterm neonates now survive infancy, there is emerging epidemiological evidence to demonstrate that individuals born preterm exhibit an elevated risk for the development of hypertension and renal impairment later in life, thus supporting the developmental origins of health and disease hypothesis. The increased risk may potentially be attributed to a negative impact of preterm birth on nephron endowment. Indeed, at the time when most preterm neonates are delivered, nephrogenesis in the kidney is still ongoing with the majority of nephrons normally formed during the third trimester of pregnancy. A number of clinical studies have provided evidence of altered renal function during the neonatal period, but to date there have been limited studies describing the consequences of preterm birth on kidney structure. Importantly, studies in the preterm baboon have shown that nephrogenesis is clearly ongoing following preterm birth; however, the presence of abnormal glomeruli (up to 18% in some cases) is of concern. Similar glomerular abnormalities have been described in autopsied preterm infants. Prenatal and postnatal factors such as exposure to certain medications, hyperoxia and intrauterine and/or extrauterine growth restriction are likely to have a significant influence on nephrogenesis and final nephron endowment. Further studies are required to determine the factors contributing to renal maldevelopment and to identify potential interventional strategies to maximize nephron endowment at the start of life, thereby optimizing long-term renal health for preterm individuals.

Keywords

preterm birth kidney nephrogenesis 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Tracy S, Tracy M, Dean J, Laws P, Sullivan E. Spontaneous preterm birth of liveborn infants in women at low risk in Australia over 10 years: a population-based study. BJOG Int J Obstetr Gynaecol. 2007;114 (6): 731–735.CrossRefGoogle Scholar
  2. 2.
    Martin J, Hamilton B, Sutton P, et al. Births: final data for 2004. Natl Vital Stat Rep. 2006;55:1–101.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Hoy WE, Hughson M, Singh GR, Douglas-Denton R, Bertram JF. Reduced nephron number and glomerulomegaly in Australian Aborigines: a group at high risk for renal disease and hypertension. Kidney Int. 2006;70 (1): 104–110.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Barker D, Osmond C, Golding J, Kuh D, Wadsworth M. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ. 1989;298 (6673): 564–567.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Rich-Edwards JW, Stampfer MJ, Manson JE, et al. Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976. BMJ. 1997;315 (7105): 396–400.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Leon DA, Johansson M, Rasmussen F. Gestational age and growth rate of fetal mass are inversely associated with systolic blood pressure in young adults: an epidemiologic study of 165, 136 Swedish men aged 18 years. Am J Epidemiol. 2000;152 (7): 597–604.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Bonamy A, Bendito A, Martin H, Andolf E, Sedin G, Norman M. Preterm birth contributes to increased vascular resistance and higher blood pressure in adolescent girls. Pediatr Res. 2005;58 (5): 845–849.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Cooper R, Atherton K, Power C. Gestational age and risk factors for cardiovascular disease: evidence from the 1958 British birth cohort followed to mid-life. Int J Epidemiol. 2009;38 (1): 235–244.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Dalziel S, Parag V, Rodgers A, Harding J. Cardiovascular risk factors at age 30 following pre-term birth. Int J Epidemiol. 2007;36 (4): 907–915.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Doyle LW, Faber B, Callanan C, Morley R. Blood pressure in late adolescence and very low birth weight. Pediatrics. 2003;111 (2): 252–257.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Hack M, Schluchter M, Cartar L, Rahman M. Blood pressure among very low birth weight (<1.5 kg) young adults. Pediatr Res. 2005;58 (4): 677–684.PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Johansson S, Iliadou A, Bergvall N, et al. Risk of high blood pressure among young men increases with the degree of immaturity at birth. Circulation. 2005;112 (22): 3430–3436.PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Kistner A, Celsi G, Vanpee M, Jacobson SH. Increased blood pressure but normal renal function in adult women born preterm. Pediatr Nephrol. 2000;15 (3–4): 215–220.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Kistner A, Jacobson L, Jacobson S, Svensson E, Hellstrom A. Low gestational age associated with abnormal retinal vascularization and increased blood pressure in adult women. Pediatr Res. 2002;51 (6): 675–680.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    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 (8 pt 1): 946–953.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Tucker J, McGuire W. Epidemiology of preterm birth. BMJ. 2004;329 (7467): 675–678.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Goldenberg R, Culhane J, Iams J, Romero R. Epidemiology and causes of preterm birth. Lancet. 2008;371 (9606): 75–84.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Kutz P, Horsch S, Kuhn L, Roll C. Single-centre vs. population-based outcome data of extremely preterm infants at the limits of viability. Acta Paediatr. 2009;98 (9): 1451–1455.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    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 (6): 777–784.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Stapleton F, Jones D, Green R. Acute renal failure in neonates: incidence, etiology and outcome. Pediatr Nephrol. 1987;1 (13): 314–320.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Hentschel R, Lodige B, Bulla M. Renal insufficiency in the neonatal period. Clin Nephrol. 1996;46 (1): 54–58.PubMedPubMedCentralGoogle Scholar
  22. 22.
    Choker G, Gouyon J. Diagnosis of acute renal failure in very preterm infants. Biol Neonate. 2004;86 (3): 212–216.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Drukker A, Guignard J. Renal aspects of the term and preterm infant: a selective update. Curr Opin Pediatr. 2002;14 (2): 175–182.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Saxen L Organogenesis of the Kidney. Cambridge: Cambridge University Press; 1987CrossRefGoogle Scholar
  25. 25.
    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.PubMedPubMedCentralGoogle Scholar
  26. 26.
    Ekblom P. Role of Extracellular Matrix in Development. Trelsatd R., ed. New York: Alan R. Liss; 1984:173–206.Google Scholar
  27. 27.
    Moritz K, Wintour E. Functional development of the meso- and metanephros. Pediatr Nephrol. 1999;13 (2): 171–178.PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Engle W. Development of fetal and neonatal renal function. Semin Perinat. 1986;10 (2): 113–124.Google Scholar
  29. 29.
    Chevalier R. Developmental renal physiology of the low birth weight pre-term newborn. J Urol. 1996;156 (2 pt 2): 714–719.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Jahnukainen T, Chen M, Berg U, Celsi G. Antenatal glucocorticoids and renal function after birth. Semin Neonatol. 2001;6 (4): 351–355.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Blackburn S Maternal, Fetal and Neonatal Physiology. Susan Blackburn, ed. St. Louis: Saunders; 2003Google Scholar
  32. 32.
    Satlin LM, Woda CB, Schwartz GJ The Kidney: From Normal Development to Congenital Disease. Vize PD Woolf A Bard JBL, ed. London: Academic Press; 2003:267–325.Google Scholar
  33. 33.
    Arant BS. Postnatal development of renal function during the first year of life. Pediatr Nephrol. 1987;1 (3): 308–313.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Ervin MG, Seidner SR, Leland MM, Ikegami M, Jobe AH. Direct fetal glucocorticoid treatment alters postnatal adaptation in premature newborn baboons. Am J Physiol. 1998;274 (4 pt 2): R1169–R1176.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Aperia A, Broberger O, Elinder G, Herin P, Zetterstrom R. Postnatal development of renal function in pre-term and full-term infants. Acta Paediatr Scand. 1981;70 (2): 183–187.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Bueva A, Guignard J. Renal function in the preterm neonate. Pedatr Res. 1994;36 (5): 572–577.CrossRefGoogle Scholar
  37. 37.
    Huang HP, Tsai IJ, Lai YC, Cheng CH, Tsau YK. Early postnatal renal growth in premature infants. Nephrology. 2007;12 (6): 572–575.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Keijzer-Veen MG, Devos AS, Meradji M, Dekker FW, Nauta J, van der Heijden BJ. Reduced renal length and volume 20 years after very preterm birth. Pediatr Nephrol. 2010;25 (3): 499–507.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    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 (5): 435–438.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Schmidt I, Chellakooty M, Boisen K, et al. Impaired kidney growth in low-birth-weight children: distinct effects of maturity and weight for gestational age. Kidney Int. 2005;68 (2): 731–740.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Faa G, Gerosa C, Fanni D, et al. Marked interindividual variability in renal maturation of preterm infants: lessons from autopsy. J Matern Fetal Neonatal Med. 2010;23 (suppl 3): 129–133.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    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 (6): F1668–F1677.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Rodriguez MM, Gomez AH, Abitbol CL, Chandar JJ, Duara S, Zilleruelo GE. Histomorphometric analysis of postnatal glomerulogenesis in extremely preterm infants. Pediatr Dev Pathol. 2004;7 (1): 17–25.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Keijzer-Veen MG, Dulger A, Dekker FW, Nauta J, van der Heijden BJ. Very preterm birth is a risk factor for increased systolic blood pressure at a young adult age. Pediatr Nephrol. 2010;25 (3): 509–516.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Hinchliffe SA, Sargent PH, Chan YF, et al. “Medullary ray glomerular counting” as a method of assessment of human nephrogenesis. Pathol Res Pract. 1992;188 (6): 775–782.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Rodriguez M, Gomez A, Abitbol C, et al. Comparative renal histomorphometry: a case study of oligonephropathy of prematurity. Pediatr Nephrol. 2005;20 (7): 945–949.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    dos Santos AM, Fonseca Ferraz ML, Pinto Rodriguez ML, et al. Assessment of renal maturity by assisted morphometry in autopsied fetuses. Early Hum Dev. 2006;82 (11): 709–713.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Gubhaju L, Black MJ. The baboon as a good model for studies of human kidney development. Pediatr Res. 2005;58 (3): 505–509.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Thomson MA, Yoder BA, Winter VT, et al. Treatment of immature baboons for 28 days with early nasal continuous positive airway pressure. Am J Respir Crit Care Med. 2004;169 (9): 1054–1062.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Bertram JF. Counting in the kidney. Kidney Int. 2001;59 (2): 792–796.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Hoy WE, Ingelfinger J, Hallan S, et al. The early development of the kidney and implications for future health. J Develop Origins Health Dis. 2010;1 (4): 216–233.CrossRefGoogle Scholar
  52. 52.
    Sutherland MR, Gubhaju L, Yoder BA, Stahlman MT, Black MJ. The effects of postnatal retinoic acid administration on nephron endowment in the preterm baboon kidney. Pediatr Res. 2009;65 (4): 397–402.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Sutherland M, Gubhaju L, Stamp L, et al. Preterm birth is associated with accelerated renal maturation and abnormalities in glomerular morphology. J Develop Origins Health Dis. 2009;1 (S1): S33–S34.Google Scholar
  54. 54.
    Siegal S, Oh W. Renal function as a marker of human fetal maturation. Acta Paediatr Scand. 1976;65 (4): 481–485.Google Scholar
  55. 55.
    Gordjani N, Burghard R, Leititis J, Brandis M. Serum creatinine and creatinine clearance in healthy neonates and prematures during the first 10 days of life. Eur J Pediatr. 1998;148 (2): 143–145.CrossRefGoogle Scholar
  56. 56.
    Awad H, el-Safty I, el-Barbary M, Imam S. Evaluation of renal glomerular and tubular functional and structural integrity in neonates. Am J Med Sci. 2002;324 (5): 261–266.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Iacobelli S, Bonsante F, Ferdinus C, Labenne M, Gouyon JB. Factors affecting postnatal changes in serum creatinine in preterm infants with gestational age <32 weeks. J Perinatol. 2009;29 (3): 232–236.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Schreuder MF, Wilhelm AJ, Bokenkamp A, et al. Impact of gestational age and birth weight on amikacin clearance on day 1 of life. Clin J Am Soc Nephrol. 2009;4 (11): 1774–1778.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Fawer CL, Torrado A, Guignard JP. Maturation of renal function in full-term and premature neonates. Helv Paediatr Acta. 1979;34 (1): 11–21.PubMedPubMedCentralGoogle Scholar
  60. 60.
    Ross B, Cowett R, Oh W. Renal functions of low birth weight infants during the first two months of life. Pediatr Res. 1977;11 (11): 1162–1164.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Gallini F, Maggio L, Romagnoli C, Marrocco G, Tortorolo G. Progression of renal function in preterm neonates with gestational age < or = 32 weeks. Pediatr Nephrol. 2000;15 (1–2): 119–124.PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Cuzzolin L, Fanos V, Pinna B, et al. Postnatal renal function in preterm newborns: a role of diseases, drugs and therapeutic interventions. Pediatr Nephrol. 2006;21 (7): 931–938.PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Stapleton F, Jones D, Green R. Acute renal failure in neonates: Incidence, etiology and outcome. Pediatr Nephrol. 1987;1 (3): 314–320.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Cuzzolin L, Fanos V, Pinna B, et al. Postnatal renal function in preterm newborns: a role of diseases, drugs and therapeutic interventions. Pediatr Nephrol. 2006;21 (7): 931–938.PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Cataldi L, Leone R, Moretti U, et al. Potential risk factors for the development of acute renal failure in preterm newborn infants: a case-control study. Arch Dis Child Fetal Neonatal Ed. 2005;90 (6): F514–F519.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Harmoinen A, Ylinen E, Ala-Houhala M, et al. Reference intervals for cystatin C in pre- and full-term infants and children. Pediatr Nephrol. 2000;15 (1–2): 105–108.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Finney H, Newman DJ, Thakkar H, Fell JM, Price CP. Reference ranges for plasma cystatin C and creatinine measurements in premature infants, neonates, and older children. Arch Dis Child. 2000;82 (1): 71–75.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Armangil D, Yurdakok M, Canpolat FE, et al. Determination of reference values for plasma cystatin C and comparison with creatinine in premature infants. Pediatr Nephrol. 2008;23 (11): 2081–2083.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Mathieson P. The cellular basis of albuminuria. Clin Sci. 2004;107 (6): 533–538.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Miner J. A molecular look at the glomerular barrier. Nephron Exp Nephrol. 2003;94:119–122.CrossRefGoogle Scholar
  71. 71.
    Davies A, Postlethwaite R, Price D, et al. Urinary albumin excretion in school children. Arch Dis Childhood. 1984;59 (7): 625–630.CrossRefGoogle Scholar
  72. 72.
    Maack T, Johnson V, Kau ST, Figueiredo J, Sigulem D. Renal filtration, transport, and metabolism of low-molecular-weight proteins: a review. Kidney Int. 1979;16 (3): 251–270.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Burghard R, Pallacks R, Gordjani N, et al. Microproteins in amniotic fluid as an index of changes in fetal renal function during development. Pediatr Nephrol. 1987;1 (4): 574–580.PubMedCrossRefPubMedCentralGoogle Scholar
  74. 74.
    Jonasson LE, Evrin PE, Wibell L. Content of beta-2-microglobulin and albumin in human amniotic fluid. A study of normal pregnancies and pregnancies complicated by haemolytic disease. Acta Obstet Gynecol Scand. 1974;53 (1): 49–58.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Takieddine F, Tabbara M, Hall P, Sokol RJ, King KC. Fetal renal maturation. Studies on urinary beta 2 microglobulin the neonate. Acta Obstet Gynecol Scand. 1983;62 (4): 311–314.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Karlsson FA, Hellsing K. Urinary protein excretion in early infancy. J Pediatr. 1976;89 (1): 89–90.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Tsukahara H, Fujii Y, Tsuchida S, et al. Renal handling of albumin and beta-2-microglobulin in neonates. Nephron. 1994;68 (2): 212–216.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Clark PM, Bryant TN, Hall MA, Lowes JA, Rowe DJ. Neonatal renal function assessment. Arch Dis Child. 1989;64 (9): 1264–1269.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Fell JM, Thakkar H, Newman DJ, Price CP. Measurement of albumin and low molecular weight proteins in the urine of newborn infants using a cotton wool ball collection method. Acta Paediatr. 1997;86 (5): 518–522.PubMedCrossRefPubMedCentralGoogle Scholar
  80. 80.
    Gubhaju L, Sutherland M, Horne R, Medhurst A, Black M Perinatal Society of Australia and New Zealand. Australia: Darwin; 2009Google Scholar
  81. 81.
    Tsukahara H, Yoshimoto M, Saito M, et al. Assessment of tubular function in neonates using urinary beta 2-microglobulin. Pediatr Nephrol. 1990;4 (5): 512–514.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Mishra J, Ma Q, Prada A, et al. Identification of neutrophil gelatinase-associated lipocalin as a novel early urinary biomarker for ischemic renal injury. J Am Soc Nephrol. 2003;14 (10): 2534–2543.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Huynh TK, Bateman DA, Parravicini E, et al. Reference values of urinary neutrophil gelatinase-associated lipocalin in very low birth weight infants. Pediatr Res. 2009;66 (5): 528–532.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Parravicini E. The clinical utility of urinary neutrophil gelatinase-associated lipocalin in the neonatal ICU. Curr Opin Pediatr. 2010;22 (2): 146–150.PubMedCrossRefPubMedCentralGoogle Scholar
  85. 85.
    Lavery AP, Meinzen-Derr JK, Anderson E, et al. Urinary NGAL in premature infants. Pediatr Res. 2008;64 (4): 423–428.PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Parravicini E, Lorenz JM, Nemerofsky SL, et al. Reference range of urinary neutrophil gelatinase-associated lipocalin in very low-birth-weight infants: preliminary data. Am J Perinatol. 2009;26 (6): 437–440.PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Zeitlin J, Ancel P, Saurel-Cubizolles M, Papiernik E. The relationship between intrauterine growth restriction and preterm delivery: an empirical approach using data from a European case-control study. BJOG Int J Obstetr Gynaecol. 2000;107 (6): 750–758.CrossRefGoogle Scholar
  88. 88.
    Manalich R, Reyes L, Herrera M, Melendi C, Fundora I. Relationship between weight at birth and the number and size of renal glomeruli in humans: a histomorphometric study. Kidney Int. 2000;58 (2): 770–773.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Hinchliffe SA, Lynch MR, Sargent PH, Howard CV, Van Velzen D. The effect of intrauterine growth retardation on the development of renal nephrons. BJOG Br J Obstetr Gynaecol. 1992;99 (4): 296–301.CrossRefGoogle Scholar
  90. 90.
    Bagby S. Maternal nutrition, low nephron number, and hypertension in later life: pathways of nutritional programming. J Nutr. 2007;137 (4): 1066–1072.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    White S, 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 (2): 248–261.PubMedCrossRefPubMedCentralGoogle Scholar
  92. 92.
    Drougia A, Giapros V, Hotoura E, et al. The effects of gestational age and growth restriction on compensatory kidney growth. Nephrol Dial Transplant. 2009;24 (1): 142–148.PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Keijzer-Veen M, Schrevel M, Finken M, et al. Microalbuminuria and lower glomerular filtration rate at young adult age in subjects born very premature and after intrauterine growth retardation. J Am Soc Nephrol. 2005;16 (9): 2762–2768.PubMedCrossRefPubMedCentralGoogle Scholar
  94. 94.
    Ehrenkranz RA. Growth outcomes of very low-birth weight infants in the newborn intensive care unit. Clin Perinatol. 2000;27 (2): 325–345.PubMedCrossRefPubMedCentralGoogle Scholar
  95. 95.
    Clark R, Thomas P, Peabody J. Extrauterine growth restriction remains a serious problem in prematurely born neonates. Pediatrics. 2003;111 (5 pt 1): 986–990.PubMedCrossRefPubMedCentralGoogle Scholar
  96. 96.
    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 (4): 445–452.PubMedCrossRefPubMedCentralGoogle Scholar
  97. 97.
    Feldman D, Carbone J, Belden L, Borgida A, Herson V. Betamethasone vs dexamethasone for the prevention of morbidity in very-low-birthweight neonates. Am J Obstet Gynecol. 2007;197 (3): 284e1–4.CrossRefGoogle Scholar
  98. 98.
    Stonestreet BS, Hansen NB, Laptook AR, Oh W. Glucocorticoid accelerates renal functional maturation in fetal lambs. Early Hum Dev. 1983;8 (3–4): 331–341.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    al-Dahan J, Stimmler L, Chantler C, Haycock GB. The effect of antenatal dexamethasone administration on glomerular filtration rate and renal sodium excretion in premature infants. Pediatr Nephrol. 1987;1 (2): 131–135.CrossRefGoogle Scholar
  100. 100.
    Kari M, Hallma M, Eronen M, et al. Prenatal dexamethasone treatment in conjunction with rescue therapy of human surfactant: a randomized placebo-controlled multicenter study. Pediatrics. 1994;93 (5): 730–736.PubMedPubMedCentralGoogle Scholar
  101. 101.
    van den Anker J, Hop W, de Groot R, et al. Effects of prenatal exposure to betamethasone and indomethacin on the glomerular filtration rate in the preterm infant. Pediatr Res. 1994;36 (5): 578–581.PubMedCrossRefPubMedCentralGoogle Scholar
  102. 102.
    Ervin M, Berry L, Ikegami M, et al. Single dose fetal betamethasone administration stabilizes postnatal glomerular filtration rate and alters endocrine function in premature lambs. Pediatr Res. 1996;40 (5): 645–651.PubMedCrossRefPubMedCentralGoogle Scholar
  103. 103.
    Challis J, Cox D, Sloboda D. Regulation of glucocorticoids in the fetus: control of birth and influence on adult disease. Semin Neonatol. 1999;4:93–97.CrossRefGoogle Scholar
  104. 104.
    Zhang J, Massmann GA, Rose JC, Figueroa JP. Differential effects of clinical doses of antenatal betamethasone on nephron endowment and glomerular filtration rate in adult sheep. Reprod Sci. 2010;17 (2): 186–195.PubMedCrossRefPubMedCentralGoogle Scholar
  105. 105.
    Ortiz L, Quan A, Weinberg A, Baum M. Effect of prenatal dexamethasone on rat renal development. Kidney Int. 2001;59 (5): 1663–1669.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Figueroa JP, Rose JC, Massmann GA, Zhang J, Acuna G. Alterations in fetal kidney development and elevations in arterial blood pressure in young adult sheep after clinical doses of antenatal glucocorticoids. Pediatr Res. 2005;58 (3): 510–515.PubMedCrossRefPubMedCentralGoogle Scholar
  107. 107.
    Celsi G, Kistner A, Aizman REA. Prenatal dexamethasone causes oligonephronia, sodium retention, and higher blood pressure in offspring. Pediatr Res. 1998;44 (3): 317–322.PubMedCrossRefPubMedCentralGoogle Scholar
  108. 108.
    Ortiz LA, Quan A, Zarzar F, Weinberg A, Baum M. Prenatal dexamethasone programs hypertension and renal injury in the rat. Hypertension. 2003;41 (2): 328–334.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    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 (pt 3): 929–935.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Fowden A, Szemere J, Hughes P, Gilmour R, Forheard A. The effects of cortisol on the growth rate of the sheep fetus during late gestation. J Endocrinol. 1996;151 (1): 97–105.PubMedCrossRefPubMedCentralGoogle Scholar
  111. 111.
    Schlabritz-Loutsevitch NE, Lopez-Alvarenga JC, Comuzzie AG, et al. The prolonged effect of repeated maternal glucocorticoid exposure on the maternal and fetal leptin/insulin-like growth factor axis in Papio species. Reprod Sci. 2009;16 (3): 308–319.PubMedCrossRefPubMedCentralGoogle Scholar
  112. 112.
    Koenen SV, Mecenas CA, Smith GS, Jenkins S, Nathanielsz PW. Effects of maternal betamethasone administration on fetal and maternal blood pressure and heart rate in the baboon at 0.7 of gestation. Am J Obstet Gynecol. 2002;186 (4): 812–817.PubMedCrossRefPubMedCentralGoogle Scholar
  113. 113.
    Miracle X, Di Renzo GC, Stark A, et al. Guideline for the use of antenatal corticosteroids for fetal maturation. J Perinat Med. 2008;36 (3): 191–196.PubMedCrossRefPubMedCentralGoogle Scholar
  114. 114.
    Gilbert T, Lelievre-Pegorier M, Merlet-Benichou C. Immediate and long-term renal effects of fetal exposure to gentamicin. Pediatr Nephrol. 1990;4 (4): 445–450.PubMedCrossRefPubMedCentralGoogle Scholar
  115. 115.
    Martinez-Salgado C, Lopez-Hernandez FJ, Lopez-Novoa JM. Glomerular nephrotoxicity of aminoglycosides. Toxicol Appl Pharmacol. 2007;223 (1): 86–98.PubMedCrossRefPubMedCentralGoogle Scholar
  116. 116.
    Nagai J, Takano M. Molecular aspects of renal handling of aminoglycosides and strategies for preventing the nephrotoxicity. Drug Metab Pharmacokinet. 2004;19 (3): 159–170.PubMedCrossRefPubMedCentralGoogle Scholar
  117. 117.
    Cullen L, Young R, Bertram J. Studies on the effects of gentamicin on rat metanephric development in vitro. Nephrology. 2000;5 (4–6): 115–123.CrossRefGoogle Scholar
  118. 118.
    Gilbert T, Gaonach S, Moreau E, Merlet-Benichou C. Defect of nephrogenesis induced by gentamicin in rat metanephric organ culture. Lab Invest. 1994;70 (5): 656–666.PubMedPubMedCentralGoogle Scholar
  119. 119.
    Giapros VI, Andronikou S, Cholevas VI, Papadopoulou ZL. Renal function in premature infants during aminoglycoside therapy. Pediatr Nephrol. 1995;9 (2): 163–166.PubMedCrossRefPubMedCentralGoogle Scholar
  120. 120.
    Giapros VI, Cholevas VI, Andronikou SK. Acute effects of gentamicin on urinary electrolyte excretion in neonates. Pediatr Nephrol. 2004;19 (3): 322–325.PubMedCrossRefPubMedCentralGoogle Scholar
  121. 121.
    Giapros V, Andronikou S, Cholevas V, Papadopoulou Z. Renal function and effect of aminoglycoside therapy during the first ten days of life. Pediatr Nephrol. 2003;18 (1): 46–52.PubMedCrossRefPubMedCentralGoogle Scholar
  122. 122.
    Elinder G, Aperia A. Development of glomerular filtration rate and excretion of beta 2-microglobulin in neonates during gentamicin treatment. Acta Paediatr Scand. 1983;72 (2): 219–224.PubMedCrossRefPubMedCentralGoogle Scholar
  123. 123.
    Rothberg AD, Andronikou S. Effect of tobramycin on fractional sodium excretion in neonates. Pediatr Pharmacol (New York). 1984;4 (1): 49–52.Google Scholar
  124. 124.
    Langhendries JP, Battisti O, Bertrand J. Aminoglycoside nephrotoxicity and urinary excretion of N-acetyl-Beta-D-glucosaminidase. Biol Neonate. 1988;53 (4): 253–259.PubMedCrossRefPubMedCentralGoogle Scholar
  125. 125.
    Kang NS, Yoo KH, Cheon H, et al. Indomethacin treatment decreases renal blood flow velocity in human neonates. Biol Neonate. 1999;76 (5): 261–265.PubMedCrossRefPubMedCentralGoogle Scholar
  126. 126.
    Andronikou S, Giapros VI, Cholevas VI, Papadopoulou ZL. Effect of aminoglycoside therapy on renal function in full-term infants. Pediatr Nephrol. 1996;10 (6): 766–768.PubMedCrossRefPubMedCentralGoogle Scholar
  127. 127.
    Tugay S, Bircan Z, Caglayan C, Arisoy AE, Gokalp AS. Acute effects of gentamicin on glomerular and tubular functions in preterm neonates. Pediatr Nephrol. 2006;21 (10): 1389–1392.PubMedCrossRefPubMedCentralGoogle Scholar
  128. 128.
    Fanos V, Mussap M, Verlato G, Plebani M, Padovani EM. Evaluation of antibiotic-induced nephrotoxicity in preterm neonates by determining urinary alpha 1-microglobulin. Pediatr Nephrol. 1996;10 (5): 645–647.PubMedCrossRefPubMedCentralGoogle Scholar
  129. 129.
    Gouyon JB, Aujard Y, Abisror A, et al. Urinary excretion of N-acetyl-glucosaminidase and beta-2-microglobulin as early markers of gentamicin nephrotoxicity in neonates. Dev Pharmacol Ther. 1987;10 (2): 145–152.PubMedCrossRefPubMedCentralGoogle Scholar
  130. 130.
    Emmanouilides G. The Ductus Arteriosus. The 75th Conference on Pediatric Research. Columbus, Ohio: Ross Laboratories; 1978Google Scholar
  131. 131.
    Ellison RC, Peckham GJ, Lang P, et al. Evaluation of the preterm infant for patent ductus arteriosus. Pediatrics. 1983;71 (3): 364–372.PubMedPubMedCentralGoogle Scholar
  132. 132.
    Moise K, Huhta J, Sharif D, et al. Indomethacin in the treatment of premature labor. Effects on the fetal ductus arteriosus. N Engl J Med. 1988;319 (6): 327–331.PubMedCrossRefPubMedCentralGoogle Scholar
  133. 133.
    Mamopoulos M, Assimakopoulos E, Reece E, et al. Maternal indomethacin therapy in the treatment of polyhydramnios. Am J Obstet Gynecol. 1990;177 (5): 256–271.Google Scholar
  134. 134.
    Giniger R, Buffat C, Millet V, Simeoni U. Renal effects of ibuprofen for the treatment of patent ductus arteriosus in premature infants. J Maternal Fetal Neonatal Med. 2007;20 (4): 275–283.CrossRefGoogle Scholar
  135. 135.
    Butler-O’Hara M, D’Angio CT. Risk of persistent renal insufficiency in premature infants following the prenatal use of indomethacin for suppression of preterm labor. J Perinatol. 2002;22 (7): 541–546.PubMedCrossRefPubMedCentralGoogle Scholar
  136. 136.
    Akima S, Kent A, Reynolds G, Gallagher M, Falk M. Indomethacin and renal impairment in neonates. Pediatr Nephrol. 2004;19 (5): 490–493.PubMedCrossRefPubMedCentralGoogle Scholar
  137. 137.
    van der Heijden BJ, Carlus C, Narcy F, et al. Persistent anuria, neonatal death, and renal microcystic lesions after prenatal exposure to indomethacin. Am J Obstet Gynecol. 1994;171 (3): 617–623.PubMedCrossRefPubMedCentralGoogle Scholar
  138. 138.
    Kaplan BS, Restaino I, Raval DS, Gottlieb RP, Bernstein J. Renal failure in the neonate associated with in utero exposure to non-steroidal anti-inflammatory agents. Pediatr Nephrol. 1994;8 (6): 700–704.PubMedCrossRefPubMedCentralGoogle Scholar
  139. 139.
    Novy M. Effects of indomethacin on labor, fetal oxygenation and fetal development in rhesus monkeys. Adv Prostaglandin Thromboxane Res. 1978;4:287–300.Google Scholar
  140. 140.
    Kent AL, Maxwell LE, Koina ME, et al. Renal glomeruli and tubular injury following indomethacin, ibuprofen, and gentamicin exposure in a neonatal rat model. Pediatr Res. 2007;62 (3): 307–312.PubMedCrossRefPubMedCentralGoogle Scholar
  141. 141.
    Kent AL, Douglas-Denton R, Shadbolt B, et al. Indomethacin, ibuprofen and gentamicin administered during late stages of glomerulogenesis do not reduce glomerular number at 14 days of age in the neonatal rat. Pediatric Nephrol. 2009;24 (6): 1143–1149.CrossRefGoogle Scholar
  142. 142.
    Saugstad OD. Oxygen and retinopathy of prematurity. J Perinatol. 2006;26 (suppl 1): S46–S50.PubMedCrossRefPubMedCentralGoogle Scholar
  143. 143.
    Chess PR, D’Angio CT, Pryhuber GS, Maniscalco WM. Pathogenesis of bronchopulmonary dysplasia. Semin Perinatol. 2006;30 (4): 171–178.PubMedCrossRefPubMedCentralGoogle Scholar
  144. 144.
    Bonamy AK, Martin H, Jorneskog G, Norman M. Lower skin capillary density, normal endothelial function and higher blood pressure in children born preterm. J Intern Med. 2007;262 (6): 635–642.PubMedCrossRefPubMedCentralGoogle Scholar
  145. 145.
    Van Blerkom J, Antczak M, Schrader R. The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels and perifollicular blood flow characteristics. Hum Reprod. 1997;12 (5): 1047–1055.PubMedCrossRefPubMedCentralGoogle Scholar
  146. 146.
    Fischer B, Bavister BD. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil. 1993;99 (2): 673–679.PubMedCrossRefPubMedCentralGoogle Scholar
  147. 147.
    Rodesch F, Simon P, Donner C, Jauniaux E. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol. 1992;80 (2): 283–285.PubMedPubMedCentralGoogle Scholar
  148. 148.
    Tufro-McReddie A, Norwood VF, Aylor KW, et al. Oxygen regulates vascular endothelial growth factor-mediated vasculogenesis and tubulogenesis. Dev Biol. 1997;183 (2): 139–149.PubMedCrossRefPubMedCentralGoogle Scholar
  149. 149.
    Yzydorczyk C, Comte B, Cambonie G, et al. Neonatal oxygen exposure in rats leads to cardiovascular and renal alterations in adulthood. Hypertension. 2008;52 (5): 889–895.PubMedCrossRefPubMedCentralGoogle Scholar
  150. 150.
    Cook NR, Cohen J, Hebert PR, Taylor JO, Hennekens CH. Implications of small reductions in diastolic blood pressure for primary prevention. Arch Intern Med. 1995;155 (7): 701–709.PubMedCrossRefPubMedCentralGoogle Scholar
  151. 151.
    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 (8): 1309–1315.PubMedCrossRefPubMedCentralGoogle Scholar
  152. 152.
    Vanpee M, Blennow M, Linne T, Herin P, Aperia A. Renal function in very low birth weight infants: normal maturity reached during early childhood. J Pediatr. 1992;121 (5 Pt 1): 784–788.PubMedCrossRefPubMedCentralGoogle Scholar
  153. 153.
    Iacobelli S, Loprieno S, Bonsante F, et al. Renal function in early childhood in very low birthweight infants. Am J Perinatol. 2007;24 (10): 587–592.PubMedCrossRefPubMedCentralGoogle Scholar
  154. 154.
    Rodriguez-Soriano J, Aguirre M, Oliveros R, Vallo A. Long-term renal follow-up of extremely low birth weight infants. Pediatr Nephrol. 2005;20 (5): 579–584.PubMedCrossRefPubMedCentralGoogle Scholar
  155. 155.
    Abitbol CL, Chandar J, Rodriguez MM, et al. Obesity and preterm birth: additive risks in the progression of kidney disease in children. Pediatr Nephrol. 2009;24 (7): 1363–1370.PubMedCrossRefPubMedCentralGoogle Scholar
  156. 156.
    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 (1): 71–76.PubMedPubMedCentralCrossRefGoogle Scholar
  157. 157.
    Vilar J, Gilbert T, Moreau E, Merlet-Benichou C. Metanephros organogenesis is highly stimulated by vitamin A derivatives in organ culture. Kidney Int. 1996;49 (5): 1478–1487.PubMedCrossRefPubMedCentralGoogle Scholar
  158. 158.
    Makrakis J, Zimanyi MA, Black MJ. Retinoic acid enhances nephron endowment in rats exposed to maternal protein restriction. Pediatr Nephrol. 2007;22 (11): 1861–1867.PubMedCrossRefPubMedCentralGoogle Scholar
  159. 159.
    Ernst KD, Radmacher PG, Rafail ST, Adamkin DH. Postnatal malnutrition of extremely low birth-weight infants with catch-up growth postdischarge. J Perinatol. 2003;23 (6): 477–482.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Society for Reproductive Investigation 2011

Authors and Affiliations

  • Lina Gubhaju
    • 1
  • Megan R. Sutherland
    • 1
  • M. Jane Black
    • 1
    Email author
  1. 1.Department of Anatomy and Developmental BiologyMonash UniversityClaytonAustralia

Personalised recommendations