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Albuminuria, renal function and blood pressure in undernourished children and recovered from undernutrition

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Abstract

Background

The objective of this study was to investigate some biomarkers of renal function and blood pressure in children who had recovered from undernutrition.

Methods

This was cross-sectional, comparative study in which a convenience sample of children of both genders (n = 126; age range 6–16 years) treated at the Centre for Nutritional Recovery and Education (São Paulo, Brazil) was used. These children were classified into four groups for analysis: (1) children who were well nourished (control group; n = 50), (2) those showing stunted growth (stunted group; n = 22), (3) those who were underweight (underweight group; n = 23) and (4) those who had recovered from undernutrition (recovered group; n = 31).

Results

No between-group differences were found for mean levels of albuminuria, serum creatinine and cystatin C, and similar mean estimates of glomerular filtration rate (eGFR; using either creatinine, cystatin C or both). Almost 14% of the stunted group, 4% of the underweight group and 3% of the recovered group had albuminuria of >30 mg/g creatinine (chi-square p = 0.034); none of the control children showed albuminuria of >30 mg/g creatinine. Mean systolic (SBP) and diastolic blood pressure (DBP) adjusted for age and gender of the children in the stunted [SBP (95% confidence interval): 92 (88–96) mmHg; DBP: 47 (44–49) mmHg] and recovered [SBP: 93 (90–96) mmHg; DBP: 49 (47–51) mmHg] groups were significantly lower than those of the controls [SBP: 98 (95–100) mmHg, P = 0.027; DBP: 53 (52–55) mmHg, P = 0.001]. After additional adjustment for height, mean DBP remained significantly lower in the recovered group compared with the control group [49 (46–51) vs. 53 (51–55) mmHg, respectively; P = 0.018). Logistic regression analysis showed that the stunted group had a 8.4-fold higher chance of developing albuminuria (>10 mg/g creatinine) than the control children (P = 0.006).

Conclusions

No alterations in renal function were found in underweight children and those who had recovered from undernutrition, whereas children with stunted growth presented with a greater risk for albuminuria. A lower DBP was found in children with stunted growth and those who had recovered from undernutrition.

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References

  1. Benabe JE, Martinez-Maldonado M (1998) The impact of malnutrition on kidney function. Min Electrolyte Metab 24:20–26

    Article  CAS  Google Scholar 

  2. Lloyd LJ, Foster T, Rhodes P, Rhind SM, Gardner DS (2012) Protein-energy malnutrition during early gestation in sheep blunts fetal renal vascular and nephron development and compromises adult renal function. J Physiol 590:377–393

    Article  CAS  PubMed  Google Scholar 

  3. Zandi-Nejad K, Luyckx VA, Brenner BM (2006) Adult hypertension and kidney disease: The role of fetal programming. Hypertension 47:502–508

    Article  CAS  PubMed  Google Scholar 

  4. Ece A, Gözü A, Bükte Y, Tutanç M, Kocamaz H (2007) The effect of malnutrition on kidney size in children. Pediatr Nephrol 22:857–863

    Article  PubMed  Google Scholar 

  5. Bacchetta J, Cochat P, Rognant N, Ranchin B, Hadj-Aissa A, Dubourg L (2011) Which creatinine and cystatin C equations can be reliably used in children? Clin J Am Soc Nephrol 6:552–560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Kidney disease: Improving Global Outcomes (KDIGO) CKD Work Group (2013) KDIGO clinical practice guideline for the evaluation and management of chronic kidney disease. Kidney Int Suppl 3:1–150

  7. Hari P, Bagga A, Mahajan P, Lakshmy R (2007) Effect of malnutrition on serum creatinine and cystatin C levels. Pediatr Nephrol 22:1757–1761

    Article  PubMed  Google Scholar 

  8. Singh A, Satchell SC (2011) Microalbuminuria: causes and implications. Pediatr Nephrol 26:1957–1965

    Article  PubMed  PubMed Central  Google Scholar 

  9. Painter RC (2004) Microalbuminuria in adults after prenatal exposure to the Dutch famine. J Am Soc Nephrol 16:189–194

    Article  PubMed  Google Scholar 

  10. Fernandes MTB, Sesso R, Martins PA, Sawaya AL (2003) Increased blood pressure in adolescents of low socioeconomic status with short stature. Pediatr Nephrol 18:435–439

    PubMed  Google Scholar 

  11. Ferreira HS, Moura FA, Cabral CR Jr, Florêncio TM, Vieira RC, de Assunção ML (2009) Short stature of mothers from an area endemic for undernutrition is associated with obesity, hypertension and stunted children: a population-based study in the semi-arid region of Alagoas, Northeast Brazil. Br J Nutr 101:1239–1245

    Article  CAS  PubMed  Google Scholar 

  12. Black RE, Victora CG, Walker SP, Bhutta ZA, Christian P, de Onis M, Ezzati M, Grantham-McGregor S, Katz J, Martorell R, Uauy R; Maternal and Child Nutrition Study Group (2013) Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet 382:427–451

  13. Martins VJB, Martins PA, das Neves J, Sawaya AL (2008) Children recovered from malnutrition exhibit normal insulin production and sensitivity. Br J Nutr 99:297–302

    Article  CAS  PubMed  Google Scholar 

  14. Neves J, Martins PA, Sesso R, Sawaya AL (2006) Malnourished children treated in day-hospital or outpatient clinics exhibit linear catch-up and normal body composition. J Nutr 136:648–655

    PubMed  Google Scholar 

  15. Martins VJB, Neves APO, do Franco CPM, Clemente AP, Sawaya AL (2014) Impact of nutritional recovery with linear growth on the concentrations of adipokines in undernourished children living in Brazilian slums. Br J Nutr 112:937–944

    Article  CAS  PubMed  Google Scholar 

  16. Martins V, Neves A, Garcia M, Spadari RC, Clemente AP, de Albuquerque MP, Hoffman DJ, Sawaya AL (2016) Normal cortisol response to cold pressor test, but lower free thyroxine, after recovery from undernutrition. Br J Nutr 115:14–23

    Article  CAS  PubMed  Google Scholar 

  17. de Alves Vieira MF, Ferraro AA, Nascimento Souza MH, Fernandes MT, Sawaya AL (2010) Height and weight gains in a nutrition rehabilitation day-care service. Public Health Nutr 13:1505–1510

    Article  Google Scholar 

  18. Weisstaub G, Araya SQM (2003) Recuperación nutricional: Un desafío pendiente. Rev Med Chil 131:213–219

    Article  PubMed  Google Scholar 

  19. World Health Organization (WHO) (1995) Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. World Health Organ Tech Rep Ser no. 854. WHO, Geneva

  20. Tanner JM (1962) The development of the reproductive system. In: Tanner JM (ed) Growth at adolescence, 2nd edn. Blackwell Scientific Publications, Oxford, pp 28–39

  21. National Institutes of Health (NIH) (2005) The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. NIH Publication No. 05-5267. https://www.nhlbi.nih.gov/files/docs/resources/heart/hbp_ped.pdf. Accessed July 2016

  22. Nobre F, Sp A, Saad CI (2010) VI Diretrizes Brasileiras VI Diretrizes Bras Hipertens. Soc Bras Cardiol 95:1–51

    Google Scholar 

  23. Schwartz GJ, Muñoz A, Schneider MF, Mak RH, Kaskel F, Warady BAFS (2009) New equations to estimate GFR in children with CKD. J Am Soc Nephrol 20:629–637

    Article  PubMed  PubMed Central  Google Scholar 

  24. Zappitelli M, Parvex P, Joseph L, Paradis G, Grey V, Lau S, Bell L (2006) Derivation and validation of cystatin C-based prediction equations for GFR in children. Am J Kidney Dis 48:221–230

    Article  CAS  PubMed  Google Scholar 

  25. Martins D, Tareen N, Zadshir A, Pan D, Vargas R, Nissenson A, Norris K (2006) The association of poverty with the prevalence of albuminuria: data from the Third National Health and Nutrition Examination Survey (NHANES III). Am J Kidney Dis 47:965–971

    Article  PubMed  Google Scholar 

  26. Sabanayagam C, Shankar A, Saw SM, Lim SC, Tai ES, Wong TY (2009) Socioeconomic status and microalbuminuria in an Asian population. Nephrol Dial Transplant 24:123–129

    Article  PubMed  Google Scholar 

  27. Yudkin JS, Phillips DI, Stanner S (1997) Proteinuria and progressive renal disease: birth weight and microalbuminuria. Nephrol Dial Transplant 12[Suppl 2]:10–13

    PubMed  Google Scholar 

  28. Salgado CM, Jardim PC, Teles FB, Nunes MC (2009) Influence of low birth weight on microalbuminuria and blood pressure of school children. Clin Nephrol 71:367–374

    Article  CAS  PubMed  Google Scholar 

  29. Simeoni U, Ligi I, Buffat C, Boubred F (2011) Adverse consequences of accelerated neonatal growth: cardiovascular and renal issues. Pediatr Nephrol 26:493–508

    Article  PubMed  Google Scholar 

  30. Menne J, Chatzikyrkou C, Haller H (2010) Microalbuminuria as a risk factor: the influence of renin-angiotensin system blockade. J Hypertens 28:1983–1994

    Article  CAS  PubMed  Google Scholar 

  31. Franco MC, Christofalo DM, Sawaya AL, Ajzen SA, Sesso R (2006) Effects of low birth weight in 8- to 13-year-old children: Implications in endothelial function and uric acid levels. Hypertension 48:45–50

    Article  CAS  PubMed  Google Scholar 

  32. Bökenkamp A, Domanetzki M, Zinck R, Schumann G, Byrd D, Brodehl J (1998) Cystatin C—a new marker of glomerular filtration rate in children independent of age and height. Pediatrics 101:875–881

    Article  PubMed  Google Scholar 

  33. Knight EL, Verhave JC, Spiegelman D, Hillege HL, de Zeeuw D, Curhan GC, de Jong PE (2004) Factors influencing serum cystatin C levels other than renal function and the impact on renal function measurement. Kidney Int 65:1416–1421

    Article  CAS  PubMed  Google Scholar 

  34. Filler G, Bökenkamp A, Hofmann W, Le Bricon T, Martínez-Brú C, Grubb A (2005) Cystatin C as a marker of GFR—history, indications, and future research. Clin Biochem 38:1–8

    Article  CAS  PubMed  Google Scholar 

  35. Hanatani S, Izumiya Y, Araki S, Rokutanda T, Kimura Y, Walsh K, Ogawa H (2014) Akt1-mediated fast/glycolytic skeletal muscle growth attenuates renal damage in experimental kidney disease. J Am Soc Nephrol 25:2800–2811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Martins PA, Hoffman DJ, Fernandes MT, Nascimento CR, Roberts SB, Sesso R, Sawaya AL (2004) Stunted children gain less lean body mass and more fat mass than their non-stunted counterparts: a prospective study. Br J Nutr 92(5):819–825

  37. Franco MCP, Nishida SK, Sesso R (2008) GFR estimated from cystatin C versus creatinine in children born small for gestational age. Am J Kidney Dis 51:925–932

    Article  CAS  PubMed  Google Scholar 

  38. Barreto GS, Vanderlei FM, Vanderlei LC, Leite ÁJ (2016) Impact of malnutrition on cardiac autonomic modulation in children. J Pediatr (Rio J) 92:638–644

    Article  Google Scholar 

  39. Febba A, Sesso R, Barreto GP, Liboni CS, Franco MC, Casarini DE (2009) Stunting growth: Association of the blood pressure levels and ACE activity in early childhood. Pediatr Nephrol 24:379–386

    Article  PubMed  Google Scholar 

  40. Sesso R, Barreto GP, Neves J, Sawaya AL (2004) Malnutrition is associated with increased blood pressure in childhood. Nephron Clin Pract 97:c61–c66

    Article  PubMed  Google Scholar 

  41. Zhang C, Shi J, Huang H, Feng LM, Ma J (2012) Nutritional status and its relationship with blood pressure among children and adolescents in South China. Eur J Pediatr 171:1073–1079

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was supported by FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo, Brazil); grant number 2010/51237-2. V. JBM was supported by CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), and ALS was supported by the CNPQ (Conselho Nacional de Desenvolvimento Científico e Tecnológico) fellowship, number 302740/2010-4. RS receives a research grant from the CNPq. FAPESP, CAPES and CNPq had no role in the design, analysis or writing of this article.

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Authors and Affiliations

  1. Department of Physiology and Pathology, Federal University of Paraíba, Centro de Ciências da Saúde, Campus I, Cidade Universitária, 58051-900, João Pessoa, PB, Brazil

    Vinicius J. B. Martins

  2. Department of Medicine, Federal University of São Paulo, Rua Botucatu, 740, 04023-900, São Paulo, SP, Brazil

    Ricardo Sesso

  3. Nutrition College, Federal University of Alagoas, Campus A. C. Simões, Avenida Lourival Melo Mota, s/n, Cidade Universitária, 57072-900, Maceió, AL, Brazil

    Ana P. G. Clemente

  4. Department of Physiology, Federal University of São Paulo, Rua Botucatu, 862, Edifício de Ciências Biomédicas, 2° andar, 04023-060, São Paulo, SP, Brazil

    Mariana B. F. Fernandes & Ana L. Sawaya

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  1. Vinicius J. B. Martins
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  2. Ricardo Sesso
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  3. Ana P. G. Clemente
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  4. Mariana B. F. Fernandes
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  5. Ana L. Sawaya
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Correspondence to Vinicius J. B. Martins.

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The authors declare that there are no conflicts of interest in this paper.

Ethical approval

The study procedures are in accordance with the principles of the Helsinki Declaration (1964) and national resolutions. All families signed the Free and Informed Consent form, and the study was approved by the Research Ethics Committee of the Federal University of São Paulo (UNIFESP-CEP 1302/09).

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Martins, V.J.B., Sesso, R., Clemente, A.P.G. et al. Albuminuria, renal function and blood pressure in undernourished children and recovered from undernutrition. Pediatr Nephrol 32, 1555–1563 (2017). https://doi.org/10.1007/s00467-017-3602-y

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  • DOI: https://doi.org/10.1007/s00467-017-3602-y

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