Advertisement

Pediatric Nephrology

, Volume 34, Issue 1, pp 137–144 | Cite as

Renal function and blood pressure are altered in adolescents born preterm

  • Andrew M. SouthEmail author
  • Patricia A. Nixon
  • Mark C. Chappell
  • Debra I. Diz
  • Gregory B. Russell
  • Elizabeth T. Jensen
  • Hossam A. Shaltout
  • T. Michael O’Shea
  • Lisa K. Washburn
Original Article

Abstract

Background

Preterm birth increases the risk of hypertension and kidney disease. However, it is unclear when changes in blood pressure (BP) and renal function become apparent and what role obesity and sex play. We hypothesized adolescents born preterm have higher BP and worse kidney function compared to term in an obesity- and sex-dependent manner.

Methods

Cross-sectional analysis of 14-year-olds born preterm with very low birth weight (n = 96) compared to term (n = 43). We used generalized linear models to estimate the associations among preterm birth and BP, estimated glomerular filtration rate (eGFR), and ln (x) urinary albumin-to-creatinine ratio (ACR), stratified by overweight/obesity (OWO, body mass index (BMI) ≥ 85th percentile) and sex.

Results

Compared to term, preterm-born adolescents had higher systolic blood pressure (SBP) and diastolic blood pressure (DBP) (adjusted β (aβ) 3.5 mmHg, 95% CI − 0.1 to 7.2 and 3.6 mmHg, 95% CI 0.1 to 7.0), lower eGFR (β − 8.2 mL/min/1.73 m2, 95% CI − 15.9 to − 0.4), and higher ACR (aβ 0.34, 95% CI − 0.04 to 0.72). OWO modified the preterm-term difference in DBP (BMI < 85th percentile aβ 5.0 mmHg, 95% CI 0.7 to 9.2 vs. OWO 0.2 mmHg, 95% CI − 5.3 to 5.6) and ACR (OWO aβ 0.72, 95% CI 0.15 to 1.29 vs. BMI < 85th percentile 0.17, 95% CI − 0.31 to 0.65). Sex modified the preterm-term ACR difference (female aβ 0.52, 95% CI 0.001 to 1.04 vs. male 0.18, 95% CI − 0.36 to 0.72).

Conclusions

Prematurity was associated with higher BP and reduced renal function that were detectable in adolescence. OWO and sex may modify the strength of these relationships.

Keywords

Chronic kidney disease Hypertension Obesity Programming Sex differences Very low birth weight 

Notes

Acknowledgements

We would like to thank the participants and their families, Patricia Brown, RN, research nurse, and Alice Scott, RN, research study coordinator. Patricia Brown and Alice Scott have no conflicts of interest.

Funding

This study is funded by the Eunice Kennedy Shriver National Institute of Child Health and Human Development (P01 HD047584; HD084227), the American Heart Association (AHA 14GRNT20480131), the Clinical Research Unit of Wake Forest Baptist Medical Center (MCRR/NIH M01-RR07122), the Wake Forest Clinical and Translational Science Award (NIH UL1 TR001420), and Forsyth Medical Center and Wake Forest School of Medicine Department of Pediatrics research funds.

Compliance with ethical standards

The Wake Forest School of Medicine and Forsyth Medical Center Institutional Review Boards approved the study. Parents or legal guardians provided written informed consent, and participants provided assent.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Kaiser JR, Tilford JM, Simpson PM, Salhab WA, Rosenfeld CR (2004) Hospital survival of very-low-birth-weight neonates from 1977 to 2000. J Perinatol 24:343–350CrossRefGoogle Scholar
  2. 2.
    Keijzer-Veen MG, Kleinveld HA, Lequin MH, Dekker FW, Nauta J, de Rijke YB, van der Heijden BJ (2007) Renal function and size at young adult age after intrauterine growth restriction and very premature birth. Am J Kidney Dis 50:542–551CrossRefGoogle Scholar
  3. 3.
    White SL, Perkovic V, Cass A, Chang CL, Poulter NR, Spector T, Haysom L, Craig JC, Salmi IA, Chadban SJ, Huxley RR (2009) Is low birth weight an antecedent of CKD in later life? A systematic review of observational studies. Am J Kidney Dis 54:248–261CrossRefGoogle Scholar
  4. 4.
    de Jong F, Monuteaux MC, van Elburg RM, Gillman MW, Belfort MB (2012) Systematic review and meta-analysis of preterm birth and later systolic blood pressure. Hypertension 59:226–234CrossRefGoogle Scholar
  5. 5.
    Brenner BM, Chertow GM (1994) Congenital oligonephropathy and the etiology of adult hypertension and progressive renal injury. Am J Kidney Dis 23:171–175CrossRefGoogle Scholar
  6. 6.
    Abitbol CL, Bauer CR, Montané B, Chandar J, Duara S, Zilleruelo G (2003) Long-term follow-up of extremely low birth weight infants with neonatal renal failure. Pediatr Nephrol 18:887–893CrossRefGoogle Scholar
  7. 7.
    Davis EF, Lazdam M, Lewandowski AJ, Worton SA, Kelly B, Kenworthy Y, Adwani S, Wilkinson AR, McCormick K, Sargent I, Redman C, Leeson P (2012) Cardiovascular risk factors in children and young adults born to preeclamptic pregnancies: a systematic review. Pediatrics 129:e1552–e1561CrossRefGoogle Scholar
  8. 8.
    Hidalgo G, Ng DK, Moxey-Mims M, Minnick ML, Blydt-Hansen T, Warady BA, Furth SL (2013) Association of income level with kidney disease severity and progression among children and adolescents with CKD: a report from the Chronic Kidney Disease in Children (CKiD) study. Am J Kidney Dis 62:1087–1094CrossRefGoogle Scholar
  9. 9.
    Ejerblad E, Fored CM, Lindblad P, Fryzek J, McLaughlin JK, Nyrén O (2006) Obesity and risk for chronic renal failure. J Am Soc Nephrol 17:1695–1702CrossRefGoogle Scholar
  10. 10.
    Li S, Chen SC, Shlipak M, Bakris G, McCullough PA, Sowers J, Stevens L, Jurkovitz C, McFarlane S, Norris K, Vassalotti J, Klag MJ, Brown WW, Narva A, Calhoun D, Johnson B, Obialo C, Whaley-Connell A, Becker B, Collins AJ (2008) Low birth weight is associated with chronic kidney disease only in men. Kidney Int 73:637–642CrossRefGoogle Scholar
  11. 11.
    Lo JC, Sinaiko A, Chandra M, Daley MF, Greenspan LC, Parker ED, Kharbanda EO, Margolis KL, Adams K, Prineas R, Magid D, O’Connor PJ (2013) Prehypertension and hypertension in community-based pediatric practice. Pediatrics 131:e415CrossRefGoogle Scholar
  12. 12.
    Oken E, Kleinman KP, Rich-Edwards J, Gillman MW (2003) A nearly continuous measure of birth weight for gestational age using a United States national reference. BMC Pediatr 3:6CrossRefGoogle Scholar
  13. 13.
    Battaglia FC, Lubchenco LO (1967) A practical classification of newborn infants by weight and gestational age. J Pediatr 71:159–163CrossRefGoogle Scholar
  14. 14.
    Barlow SE (2007) Expert committee recommendations regarding the prevention, assessment, and treatment of child and adolescent overweight and obesity: summary report. Pediatrics 120(Suppl 4):S164–S192CrossRefGoogle Scholar
  15. 15.
    Taylor SJ, Whincup PH, Hindmarsh PC, Lampe F, Odoki K, Cook DG (2001) Performance of a new pubertal self-assessment questionnaire: a preliminary study. Paediatr Perinat Epidemiol 15:88–94CrossRefGoogle Scholar
  16. 16.
    National High Blood Pressure Education Program Working Group on Hypertension Control in Children and Adolescents (1996) Update on the 1987 Task Force Report on High Blood Pressure in Children and Adolescents: a working group report from the National High Blood Pressure Education Program. Pediatrics 98:649–658Google Scholar
  17. 17.
    Rosner B, Cook N, Portman R, Daniels S, Falkner B (2008) Determination of blood pressure percentiles in normal-weight children: some methodological issues. Am J Epidemiol 167:653–666CrossRefGoogle Scholar
  18. 18.
    Flynn JT, Kaelber DC, Baker-Smith CM, Blowey D, Carroll AE, Daniels SR, de Ferranti SD, Dionne JM, Falkner B, Flinn SK, Gidding SS, Goodwin C, Leu MG, Powers ME, Rea C, Samuels J, Simasek M, Thaker VV, Urbina EM (2017) Clinical practice guideline for screening and management of high blood pressure in children and adolescents. Pediatrics 140:e20171904CrossRefGoogle Scholar
  19. 19.
    Schwartz GJ, Brion LP, Spitzer A (1987) The use of plasma creatinine concentration for estimating glomerular filtration rate in infants, children, and adolescents. Pediatr Clin N Am 34:571–590CrossRefGoogle Scholar
  20. 20.
    Rademacher ER, Sinaiko AR (2009) Albuminuria in children. Curr Opin Nephrol Hypertens 18:246–251CrossRefGoogle Scholar
  21. 21.
    Shrier I, Platt RW (2008) Reducing bias through directed acyclic graphs. BMC Med Res Methodol 8:70CrossRefGoogle Scholar
  22. 22.
    Vashishta N, Surapaneni V, Chawla S, Kapur G, Natarajan G (2017) Association among prematurity (<30 weeks’ gestational age), blood pressure, urinary albumin, calcium, and phosphate in early childhood. Pediatr Nephrol 32:1243–1250CrossRefGoogle Scholar
  23. 23.
    Parkinson JRC, Hyde MJ, Gale C, Santhakumaran S, Modi N (2013) Preterm birth and the metabolic syndrome in adult life: a systematic review and meta-analysis. Pediatrics 131:e1240–e1263CrossRefGoogle Scholar
  24. 24.
    Simonetti GD, Raio L, Surbek D, Nelle M, Frey FJ, Mohaupt MG (2008) Salt sensitivity of children with low birth weight. Hypertension 52:625–630CrossRefGoogle Scholar
  25. 25.
    Nixon PA, Washburn LK, O’Shea TM, Shaltout HA, Russell GB, Snively BM, Rose JC (2017) Antenatal steroid exposure and heart rate variability in adolescents born with very low birth weight. Pediatr Res 81:57–62CrossRefGoogle Scholar
  26. 26.
    Washburn LK, Chappell MC, Beavers D, Diz DI, Jensen ET, Nixon PA, Shaltout HA, South AM, Taylor RN, Rose JC (2017) Adult males of very low birth weight with antenatal corticosteroid exposure exhibit an enhanced blood pressure response to acute stress [abstract]. FASEB J 31(Suppl 1):852.8Google Scholar
  27. 27.
    Washburn LK, Nixon PA, Russell GB, Snively BM, O’Shea TM (2015) Preterm birth is associated with higher uric acid levels in adolescents. J Pediatr 167:76–80CrossRefGoogle Scholar
  28. 28.
    South AM, Nixon PA, Chappell MC, Diz DI, Russell GB, Jensen ET, Shaltout HA, O’Shea TM, Washburn LK (2018) Association between preterm birth and the renin−angiotensin system in adolescence: influence of sex and obesity. J Hypertens.  https://doi.org/10.1097/hjh.0000000000001801 CrossRefGoogle Scholar
  29. 29.
    South AM, Nixon PN, Chappell MC, Diz DI, Jensen ET, Shaltout HA, Washburn LK (2018) Urinary α-klotho is associated with higher blood pressure and reduced urinary angiotensin-(1-7) in young adults born preterm [abstract]. Pediatr Acad Soc E-PAS2018:1502.1841Google Scholar
  30. 30.
    Skilton MR, Viikari JSA, Juonala M, Laitinen T, Lehtimäki T, Taittonen L, Kähönen M, Celermajer DS, Raitakari OT (2011) Fetal growth and preterm birth influence cardiovascular risk factors and arterial health in young adults: the Cardiovascular Risk in Young Finns study. Arterioscler Thromb Vasc Biol 31:2975–2981CrossRefGoogle Scholar
  31. 31.
    Juonala M, Magnussen CG, Berenson GS, Venn A, Burns TL, Sabin MA, Srinivasan SR, Daniels SR, Davis PH, Chen W, Sun C, Cheung M, Viikari JSA, Dwyer T, Raitakari OT (2011) Childhood adiposity, adult adiposity, and cardiovascular risk factors. N Engl J Med 365:1876–1885CrossRefGoogle Scholar
  32. 32.
    Kwinta P, Klimek M, Drozdz D, Grudzień A, Jagła M, Zasada M, Pietrzyk JJ (2011) Assessment of long-term renal complications in extremely low birth weight children. Pediatr Nephrol 26:1095–1103CrossRefGoogle Scholar
  33. 33.
    Starzec K, Klimek M, Grudzień A, Jagła M, Kwinta P (2016) Longitudinal assessment of renal size and function in extremely low birth weight children at 7 and 11 years of age. Pediatr Nephrol 31:2119–2126CrossRefGoogle Scholar
  34. 34.
    Hodgin JB, Rasoulpour M, Markowitz GS, D’Agati VD (2009) Very low birth weight is a risk factor for secondary focal segmental glomerulosclerosis. Clin J Am Soc Nephrol 4:71–76CrossRefGoogle Scholar
  35. 35.
    Sutherland MR, Gubhaju L, Moore L, Kent AL, Dahlstrom JE, Horne RSC, Hoy WE, Bertram JF, Black MJ (2011) Accelerated maturation and abnormal morphology in the preterm neonatal kidney. J Am Soc Nephrol 22:1365–1374CrossRefGoogle Scholar
  36. 36.
    Curhan GC, Chertow GM, Willett WC, Spiegelman D, Colditz GA, Manson JE, Speizer FE, Stampfer MJ (1996) Birth weight and adult hypertension and obesity in women. Circulation 94:1310–1315CrossRefGoogle Scholar
  37. 37.
    Tsuboi N, Okabayashi Y, Shimizu A, Yokoo T (2017) The renal pathology of obesity. Kidney Int Rep 2:251–260CrossRefGoogle Scholar
  38. 38.
    Puelles VG, Douglas-Denton RN, Zimanyi MA, Armitage JA, Hughson MD, Kerr PG, Bertram JF (2014) Glomerular hypertrophy in subjects with low nephron number: contributions of sex, body size and race. Nephrol Dial Transplant 29:1686–1695CrossRefGoogle Scholar
  39. 39.
    Mian AN, Schwartz GJ (2017) Measurement and estimation of glomerular filtration rate in children. Adv Chronic Kidney Dis 24:348–356CrossRefGoogle Scholar
  40. 40.
    Pottel H (2017) Measuring and estimating glomerular filtration rate in children. Pediatr Nephrol 32:249–263CrossRefGoogle Scholar
  41. 41.
    Schwartz GJ, Muñoz A, Schneider MF, Mak RH, Kaskel F, Warady BA, Furth SL (2009) New equations to estimate GFR in children with CKD. J Am Soc Nephrol 20:629–637CrossRefGoogle Scholar

Copyright information

© IPNA 2018

Authors and Affiliations

  • Andrew M. South
    • 1
    • 2
    • 3
    Email author
  • Patricia A. Nixon
    • 1
    • 4
  • Mark C. Chappell
    • 2
    • 5
  • Debra I. Diz
    • 2
    • 5
  • Gregory B. Russell
    • 6
  • Elizabeth T. Jensen
    • 3
  • Hossam A. Shaltout
    • 2
    • 7
    • 8
  • T. Michael O’Shea
    • 9
  • Lisa K. Washburn
    • 1
    • 2
  1. 1.Department of PediatricsWake Forest School of MedicineWinston-SalemUSA
  2. 2.Cardiovascular Sciences CenterWake Forest School of MedicineWinston-SalemUSA
  3. 3.Division of Public Health Sciences, Department of Epidemiology and PreventionWake Forest School of MedicineWinston-SalemUSA
  4. 4.Department of Health and Exercise ScienceWake Forest UniversityWinston-SalemUSA
  5. 5.Department of Surgery-Hypertension and Vascular ResearchWake Forest School of MedicineWinston-SalemUSA
  6. 6.Division of Public Health Sciences, Department of Biostatistical SciencesWake Forest School of MedicineWinston-SalemUSA
  7. 7.Department of Obstetrics and GynecologyWake Forest School of MedicineWinston-SalemUSA
  8. 8.Department of Pharmacology and Toxicology, School of PharmacyUniversity of AlexandriaAlexandriaEgypt
  9. 9.Department of PediatricsUniversity of North Carolina School of MedicineChapel HillUSA

Personalised recommendations