Vitamin and trace element deficiencies in the pediatric dialysis patient

  • Lyndsay A. Harshman
  • Kathy Lee-Son
  • Jennifer G. Jetton
Educational Review

Abstract

Pediatric dialysis patients are at risk of nutritional illness secondary to deficiencies in water-soluble vitamins and trace elements. Unlike 25-OH vitamin D, most other vitamins and trace elements are not routinely monitored in the blood and, consequently, the detection of any deficiency may not occur until significant complications develop. Causes of vitamin and trace element deficiency in patients on maintenance dialysis patient are multifactorial, ranging from diminished nutritional intake to altered metabolism as well as dialysate-driven losses of water-soluble vitamins and select trace elements. In this review we summarize the nutritional sources of key water-soluble vitamins and trace elements with a focus on the biological roles and clinical manifestations of their respective deficiency to augment awareness of potential nutritional illness in pediatric patients receiving maintenance dialysis. The limited pediatric data on the topic of clearance of water-soluble vitamins and trace elements by individual dialysis modality are reviewed, including a brief discussion on clearance of water-soluble vitamins and trace elements with continuous renal replacement therapy.

Keywords

Nutritional illness Water-soluble vitamins Wernicke encephalopathy Zinc Selenium Clearance 

References

  1. 1.
    Ratsch IM, Catassi C, Verrina E, Gusmano R, Appiani A, Bettinelli A, Picca S, Rizzoni G, Fabian-Bach C, Wingen AM, Mehls O, Giorgi PL (1992) Energy and nutrient intake of patients with mild-to-moderate chronic renal failure compared with healthy children: an Italian multicentre study. Eur J Pediatr 151:701–705CrossRefPubMedGoogle Scholar
  2. 2.
    Norman LJ, Coleman JE, Macdonald IA, Tomsett AM, Watson AR (2000) Nutrition and growth in relation to severity of renal disease in children. Pediatr Nephrol 15:259–265CrossRefPubMedGoogle Scholar
  3. 3.
    Makoff R (1991) Water-soluble vitamin status in patients with renal disease treated with hemodialysis or peritoneal dialysis. J Renal Nutr 1:56–73CrossRefGoogle Scholar
  4. 4.
    Makoff R, Dwyer J, Rocco MV (1996) Folic acid, pyridoxine, cobalamin, and homocysteine and their relationship to vardiovascular disease in end-stage renal disease. J Renal Nutr 6:2–11CrossRefGoogle Scholar
  5. 5.
    Kleinman RE, Greer FR (2013) Trace elements. Pediatric nutrition. American Academy of Pediatrics, Elk Grove VillageGoogle Scholar
  6. 6.
    National Kidney Foundation (2009) KDOQI clinical practice guideline for nutrition in children with CKD: 2008 update. Am J Kidney Dis 53(Suppl 2):S1-123Google Scholar
  7. 7.
    Minister of Public Works and Government Services (2010) Dietary reference intake: recommended dietary allowance and adequate intake: Health Canada. Available from:https://www.canada.ca/en/health-canada/services/food-nutrition/healthy-eating/dietary-reference-intakes/tables.html. Accessed 5 Jan 2017
  8. 8.
    Kriley M, Warady BA (1991) Vitamin status of pediatric patients receiving long-term peritoneal dialysis. Am J Clin Nutr 53:1476–1479PubMedGoogle Scholar
  9. 9.
    Warady BA, Kriley M, Alon U, Hellerstein S (1994) Vitamin status of infants receiving long-term peritoneal dialysis. Pediatr Nephrol 8:354–356CrossRefPubMedGoogle Scholar
  10. 10.
    Wiesen P, Van Overmeire L, Delanaye P, Dubois B, Preiser JC (2011) Nutrition disorders during acute renal failure and renal replacement therapy. J Parenter Enteral Nutr 35:217–222CrossRefGoogle Scholar
  11. 11.
    Wang AY, Sea MM, Ip R, Law MC, Chow KM, Lui SF, Li PK, Woo J (2002) Independent effects of residual renal function and dialysis adequacy on dietary micronutrient intakes in patients receiving continuous ambulatory peritoneal dialysis. Am J Clin Nutr 76:569–576PubMedGoogle Scholar
  12. 12.
    Berger MM, Shenkin A, Revelly JP, Roberts E, Cayeux MC, Baines M, Chiolero RL (2004) Copper, selenium, zinc, and thiamine balances during continuous venovenous hemodiafiltration in critically ill patients. Am J Clin Nutr 80:410–416PubMedGoogle Scholar
  13. 13.
    Sequeira Lopes da Silva JT, Almaraz Velarde R, Olgado Ferrero F, Robles Marcos M, Perez Civantos D, Ramirez Moreno JM, Luengo Perez LM (2010) Wernicke’s encephalopathy induced by total parental nutrition. Nutr Hosp 25:1034–1036PubMedGoogle Scholar
  14. 14.
    Francini-Pesenti F, Brocadello F, Manara R, Santelli L, Laroni A, Caregaro L (2009) Wernicke’s syndrome during parenteral feeding: not an unusual complication. Nutrition 25:142–146CrossRefPubMedGoogle Scholar
  15. 15.
    Chazot C, Kopple JD (2003) Vitamin metabolism and requirements in renal disease and renal failure. In: Kopple JD, Massry SG (eds) Kopple and Massry’s nutritional management of renal disease. Lippincott Williams & Wilkins, Philadelphia, pp 415–478Google Scholar
  16. 16.
    Cavadini C, Siega-Riz AM, Popkin BM (2000) US adolescent food intake trends from 1965 to 1996. West J Med 173:378–383CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Jankowska M, Szupryczynska N, Debska-Slizien A, Borek P, Kaczkan M, Rutkowski B, Malgorzewicz S (2016) Dietary intake of vitamins in different options of treatment in chronic kidney disease: is there a deficiency? Transplant Proc 48:1427–1430CrossRefPubMedGoogle Scholar
  18. 18.
    Foreman JW, Abitbol CL, Trachtman H, Garin EH, Feld LG, Strife CF, Massie MD, Boyle RM, Chan JC (1996) Nutritional intake in children with renal insufficiency: a report of the growth failure in children with renal diseases study. J Am Coll Nutr 15:579–585CrossRefPubMedGoogle Scholar
  19. 19.
    Raimann JG, Levin NW, Craig RG, Sirover W, Kotanko P, Handelman G (2013) Is vitamin C intake too low in dialysis patients? Semin Dial 26:1–5CrossRefPubMedGoogle Scholar
  20. 20.
    Jackson P, Loughrey CM, Lightbody JH, McNamee PT, Young IS (1995) Effect of hemodialysis on total antioxidant capacity and serum antioxidants in patients with chronic renal failure. Clin Chem 41:1135–1138PubMedGoogle Scholar
  21. 21.
    Rolton HA, McConnell KM, Modi KS, Macdougall AI (1991) The effect of vitamin C intake on plasma oxalate in patients on regular haemodialysis. Nephrol Dial Transplant 6:440–443CrossRefPubMedGoogle Scholar
  22. 22.
    Ono K (1986) Secondary hyperoxalemia caused by vitamin C supplementation in regular hemodialysis patients. Clin Nephrol 26:239–243PubMedGoogle Scholar
  23. 23.
    Kuramoto Y, Igarashi Y, Tagami H (1991) Acquired zinc deficiency in breast-fed infants. Semin Dermatol 10:309–312PubMedGoogle Scholar
  24. 24.
    Piela Z, Szuber M, Mach B, Janniger CK (1998) Zinc deficiency in exclusively breast-fed infants. Cutis 61:197–200PubMedGoogle Scholar
  25. 25.
    Erdman JW Jr, Fordyce EJ (1989) Soy products and the human diet. Am J Clin Nutr 49:725–737PubMedGoogle Scholar
  26. 26.
    Sandstrom B, Cederblad A, Lonnerdal B (1983) Zinc absorption from human milk, cow’s milk, and infant formulas. Am J Dis Child 137:726–729PubMedGoogle Scholar
  27. 27.
    Vinceti M, Filippini T, Cilloni S, Bargellini A, Vergoni AV, Tsatsakis A, Ferrante M (2017) Health risk assessment of environmental selenium: emerging evidence and challenges (review). Mol Med Rep 15:3323–3335PubMedPubMedCentralGoogle Scholar
  28. 28.
    Velez RJ, Myers B, Guber MS (1985) Severe acute metabolic-acidosis (acute beriberi)—an avoidable complication of total parenteral-nutrition. J Parenter Enter 9:216–219CrossRefGoogle Scholar
  29. 29.
    Giacalone M, Martinelli R, Abramo A, Rubino A, Pavoni V, Iacconi P, Giunta F, Forfori F (2015) Rapid reversal of severe lactic acidosis after thiamine administration in critically ill adults: a report of 3 cases. Nutr Clin Pract 30:104–110CrossRefPubMedGoogle Scholar
  30. 30.
    Hung SC, Hung SH, Tarng DC, Yang WC, Chen TW, Huang TP (2001) Thiamine deficiency and unexplained encephalopathy in hemodialysis and peritoneal dialysis patients. Am J Kidney Dis 38:941–947CrossRefPubMedGoogle Scholar
  31. 31.
    Descombes E, Dessibourg CA, Fellay G (1991) Acute encephalopathy due to thiamine deficiency (Wernicke’s encephalopathy) in a chronic hemodialyzed patient: a case report. Clin Nephrol 35:171–175PubMedGoogle Scholar
  32. 32.
    Barbara PG, Manuel B, Elisabetta M, Giorgio S, Fabio T, Valentina C, Emanuela M, Massimo B, Giuseppe S, Paolo SG (2006) The suddenly speechless florist on chronic dialysis: the unexpected threats of a flower shop? Diagnosis: dialysis related Wernicke encephalopathy. Nephrol Dial Transplant 21:223–225CrossRefPubMedGoogle Scholar
  33. 33.
    Dyckner T, Ek B, Nyhlin H, Wester PO (1985) Aggravation of thiamine deficiency by magnesium depletion. A case report. Acta Med Scand 218:129–131CrossRefPubMedGoogle Scholar
  34. 34.
    Koury MJ, Horne DW (1994) Apoptosis mediates and thymidine prevents erythroblast destruction in folate deficiency anemia. Proc Natl Acad Sci USA 91:4067–4071CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Shenkin A, Roberts NB, Chem C (2012) Vitamins and trace elements. In: Burtis CA, Ashwood ER, Bruns DE (eds) Teitz textbook of clinical chemistry and molecular diagnostics. Saunders/Elsevier, St. LouisGoogle Scholar
  36. 36.
    Nankivell BJ (1991) Vitamin B6 deficiency on hemodialysis causing sideroblastic anemia. Nephron 59:674–675CrossRefPubMedGoogle Scholar
  37. 37.
    Bamgbola OF, Kaskel F (2005) Role of folate deficiency on erythropoietin resistance in pediatric and adolescent patients on chronic dialysis. Pediatr Nephrol 20:1622–1629CrossRefPubMedGoogle Scholar
  38. 38.
    Ducker GS, Rabinowitz JD (2016) One-carbon metabolism in health and disease. Cell Metab 25:27–42CrossRefPubMedGoogle Scholar
  39. 39.
    Jamison RL, Hartigan P, Kaufman JS, Goldfarb DS, Warren SR, Guarino PD, Gaziano JM, Veterans Affairs Site I (2007) Effect of homocysteine lowering on mortality and vascular disease in advanced chronic kidney disease and end-stage renal disease: a randomized controlled trial. JAMA 298:1163–1170CrossRefPubMedGoogle Scholar
  40. 40.
    Heinz J, Kropf S, Domrose U, Westphal S, Borucki K, Luley C, Neumann KH, Dierkes J (2010) B vitamins and the risk of total mortality and cardiovascular disease in end-stage renal disease: results of a randomized controlled trial. Circulation 121:1432–1438CrossRefPubMedGoogle Scholar
  41. 41.
    Schroder CH, de Boer AW, Giesen AM, Monnens LA, Blom H (1999) Treatment of hyperhomocysteinemia in children on dialysis by folic acid. Pediatr Nephrol 13:583–585CrossRefPubMedGoogle Scholar
  42. 42.
    Pinnell SR (1985) Regulation of collagen biosynthesis by ascorbic acid: a review. Yale J Biol Med 58:553–559PubMedPubMedCentralGoogle Scholar
  43. 43.
    Murad S, Grove D, Lindberg KA, Reynolds G, Sivarajah A, Pinnell SR (1981) Regulation of collagen synthesis by ascorbic acid. Proc Natl Acad Sci USA 78:2879–2882CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Fidler MC, Davidsson L, Zeder C, Walczyk T, Hurrell RF (2003) Iron absorption from ferrous fumarate in adult women is influenced by ascorbic acid but not by Na2EDTA. Br J Nutr 90:1081–1085CrossRefPubMedGoogle Scholar
  45. 45.
    Handelman GJ (2011) New insight on vitamin C in patients with chronic kidney disease. J Ren Nutr 21:110–112CrossRefPubMedGoogle Scholar
  46. 46.
    Kittisakmontri K, Swangtrakul N, Padungmaneesub W, Charoenkwan P (2016) Gingival bleeding and bloody dialysate: a case report of scurvy in a child with end-stage renal disease receiving peritoneal dialysis. J Ren Nutr 26:407–411CrossRefPubMedGoogle Scholar
  47. 47.
    Stefanidou M, Maravelias C, Dona A, Spiliopoulou C (2006) Zinc: a multipurpose trace element. Arch Toxicol 80:1–9CrossRefPubMedGoogle Scholar
  48. 48.
    Berg JM, Shi Y (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science 271:1081–1085CrossRefPubMedGoogle Scholar
  49. 49.
    Lee SH, Huang JW, Hung KY, Leu LJ, Kan YT, Yang CS, Wu DC, Huang CL, Chen PY, Chen JS, Chen WY (2000) Trace metals’ abnormalities in hemodialysis patients: relationship with medications. Artif Organs 24:841–844CrossRefPubMedGoogle Scholar
  50. 50.
    Vanholder R, Cornelis R, Dhondt A, Lameire N (2002) The role of trace elements in uraemic toxicity. Nephrol Dial Transplant 17(Suppl 2):2–8CrossRefPubMedGoogle Scholar
  51. 51.
    Yang CY, Wu ML, Chou YY, Li SY, Deng JF, Yang WC, Ng YY (2012) Essential trace element status and clinical outcomes in long-term dialysis patients: a two-year prospective observational cohort study. Clin Nutr 31:630–636CrossRefPubMedGoogle Scholar
  52. 52.
    Shankar AH, Prasad AS (1998) Zinc and immune function: the biological basis of altered resistance to infection. Am J Clin Nutr 68:447S–463SPubMedGoogle Scholar
  53. 53.
    Chen J, Wang S, Luo M, Zhang Z, Dai X, Kong M, Cai L, Wang Y, Shi B, Tan Y (2016) Zinc deficiency worsens and supplementation prevents high-fat diet induced vascular inflammation, oxidative stress, and pathological remodeling. Toxicol Sci 153(1):124–136Google Scholar
  54. 54.
    Prasad AS (1985) Clinical manifestations of zinc deficiency. Annu Rev Nutr 5:341–363CrossRefPubMedGoogle Scholar
  55. 55.
    Parra E, Campistol JM, Soy D, Deulofeu R (1995) Acrodermatitis enteropathica-like syndrome in a dialysis patient. Nephron 70:389–390CrossRefPubMedGoogle Scholar
  56. 56.
    Turan B, Delilbasi E, Dalay N, Sert S, Afrasyap L, Sayal A (1992) Serum selenium and glutathione-peroxidase activities and their interaction with toxic metals in dialysis and renal-transplantation patients. Biol Trace Elem Res 33:95–102CrossRefPubMedGoogle Scholar
  57. 57.
    Chen J, Berry MJ (2003) Selenium and selenoproteins in the brain and brain diseases. J Neurochem 86:1–12CrossRefPubMedGoogle Scholar
  58. 58.
    Rederstorff M, Krol A, Lescure A (2006) Understanding the importance of selenium and selenoproteins in muscle function. Cell Mol Life Sci 63:52–59CrossRefPubMedGoogle Scholar
  59. 59.
    Liu ML, Xu G, Huang ZY, Zhong XC, Liu SH, Jiang TY (2011) Euthyroid sick syndrome and nutritional status are correlated with hyposelenemia in hemodialysis patients. Int J Artif Organs 34:577–583CrossRefPubMedGoogle Scholar
  60. 60.
    D’Haese PC, De Broe ME (1996) Adequacy of dialysis: trace elements in dialysis fluids. Nephrol Dial Transplant 11(Suppl 2):92–97CrossRefPubMedGoogle Scholar
  61. 61.
    Heinz J, Domrose U, Westphal S, Luley C, Neumann KH, Dierkes J (2008) Washout of water-soluble vitamins and of homocysteine during haemodialysis: effect of high-flux and low-flux dialyser membranes. Nephrology 13:384–389CrossRefPubMedGoogle Scholar
  62. 62.
    Vanrenterghem D, Cornelis R, Vanholder R (1992) Behavior of 12 trace-elements in serum of uremic patients on Hemodiafiltration. J Trace Elem Electrolytes Health Dis 6:169–174Google Scholar
  63. 63.
    Fouque D, Vennegoor M, ter Wee P, Wanner C, Basci A, Canaud B, Haage P, Konner K, Kooman J, Martin-Malo A, Pedrini L, Pizzarelli F, Tattersall J, Tordoir J, Vanholder R (2007) EBPG guideline on nutrition. Nephrol Dial Transplant 22(Suppl 2):Sii45–Sii87Google Scholar
  64. 64.
    Ueda K, Takada D, Mii A, Tsuzuku Y, Saito SK, Kaneko T, Utsumi K, Iino Y, Katayama Y (2006) Severe thiamine deficiency resulted in Wernicke’s encephalopathy in a chronic dialysis patient. Clin Exp Nephrol 10:290–293CrossRefPubMedGoogle Scholar
  65. 65.
    Corken M, Porter J (2011) Is vitamin B(6) deficiency an under-recognized risk in patients receiving haemodialysis? A systematic review: 2000–2010. Nephrology (Carlton) 16:619–625Google Scholar
  66. 66.
    Kasama R, Koch T, Canals-Navas C, Pitone JM (1996) Vitamin B6 and hemodialysis: the impact of high-flux/high-efficiency dialysis and review of the literature. Am J Kidney Dis 27:680–686CrossRefPubMedGoogle Scholar
  67. 67.
    Leblanc M, Pichette V, Geadah D, Ouimet D (2000) Folic acid and pyridoxal-5′-phosphate losses during high-efficiency hemodialysis in patients without hydrosoluble vitamin supplementation. J Ren Nutr 10:196–201CrossRefPubMedGoogle Scholar
  68. 68.
    Richter A, Kuhlmann MK, Seibert E, Kotanko P, Levin NW, Handelman GJ (2008) Vitamin C deficiency and secondary hyperparathyroidism in chronic haemodialysis patients. Nephrol Dial Transplant 23:2058–2063CrossRefPubMedGoogle Scholar
  69. 69.
    Zhang KY, Dong J, Cheng XY, Bai WY, Guo WY, Wu LY, Zuo L (2012) Association between vitamin C deficiency and dialysis modalities. Nephrology 17:452–457CrossRefPubMedGoogle Scholar
  70. 70.
    Morena M, Cristol JP, Bosc JY, Tetta C, Forret G, Leger CL, Delcourt C, Papoz L, Descomps B, Canaud B (2002) Convective and diffusive losses of vitamin C during haemodiafiltration session: a contributive factor to oxidative stress in haemodialysis patients. Nephrol Dial Transplant 17:422–427CrossRefPubMedGoogle Scholar
  71. 71.
    Bohm V, Tiroke K, Schneider S, Sperschneider H, Stein G, Bitsch R (1997) Vitamin C status of patients with chronic renal failure, dialysis patients and patients after renal transplantation. Int J Vitam Nutr Res 67:262–266PubMedGoogle Scholar
  72. 72.
    Sullivan JF, Eisenstein AB (1972) Ascorbic acid depletion during hemodialysis. JAMA 220:1697–1699CrossRefPubMedGoogle Scholar
  73. 73.
    Coveney N, Polkinghorne KR, Linehan L, Corradini A, Kerr PG (2011) Water-soluble vitamin levels in extended hours hemodialysis. Hemodial Int 15:30–38CrossRefPubMedGoogle Scholar
  74. 74.
    Bhogade RB, Suryakar AN, Joshi NG (2013) Effect of hemodialysis on serum copper and zinc levels in renal failure patients. Eur J Gen Med 10:154–157Google Scholar
  75. 75.
    Guo CH, Wang CL (2013) Effects of zinc supplementation on plasma copper/zinc ratios, oxidative stress, and immunological status in hemodialysis patients. Int J Med Sci 10:79–89CrossRefPubMedGoogle Scholar
  76. 76.
    Tonelli M, Wiebe N, Hemmelgarn B, Klarenbach S, Field C, Manns B, Thadhani R, Gill J, The Alberta Kidney Disease Network (2009) Trace elements in hemodialysis patients: a systematic review and meta-analysis. BMC Med 7:25CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Bober J, Kwiatkowska E, Kedzierska K, Olszewska M, Golebiewska E, Stachowska E, Kucharska E, Ciechanowski K, Chlubek D (2007) Influence of glucose in the dialysate on the activity of erythrocyte-glutathione-peroxidase and blood selenium concentration in hemodialyzed patients. Arch Med Res 38:330–336CrossRefPubMedGoogle Scholar
  78. 78.
    Iglesias SB, Leite HP, Paes AT, Oliveira SV, Sarni RO (2014) Low plasma selenium concentrations in critically ill children: the interaction effect between inflammation and selenium deficiency. Crit Care 18:R101CrossRefPubMedGoogle Scholar
  79. 79.
    Blumberg A, Hanck A, Sander G (1983) Vitamin nutrition in patients on continuous ambulatory peritoneal-dialysis (CAPD). Clin Nephrol 20:244–250PubMedGoogle Scholar
  80. 80.
    Boeschoten EW, Schrijver J, Krediet RT, Schreurs WH, Arisz L (1988) Deficiencies of vitamins in CAPD patients: the effect of supplementation. Nephrol Dial Transplant 3:187–193PubMedGoogle Scholar
  81. 81.
    Makoff R (1999) Vitamin replacement therapy in renal failure patients. Miner Electrolyte Metab 25:349–351CrossRefPubMedGoogle Scholar
  82. 82.
    Tsapas G, Magoula I, Paletas K, Concouris L (1983) Effect of peritoneal dialysis on plasma levels of ascorbic acid. Nephron 33:34–37CrossRefPubMedGoogle Scholar
  83. 83.
    Sriram K, Abraham G (2000) Loss of zinc and selenium does not occur through peritoneal dialysis. Nutrition 16:1047–1051CrossRefPubMedGoogle Scholar
  84. 84.
    Story DA, Ronco C, Bellomo R (1999) Trace element and vitamin concentrations and losses in critically ill patients treated with continuous venovenous hemofiltration. Crit Care Med 27:220–223CrossRefPubMedGoogle Scholar
  85. 85.
    Zappitelli M, Juarez M, Castillo L, Coss-Bu J, Goldstein SL (2009) Continuous renal replacement therapy amino acid, trace metal and folate clearance in critically ill children. Intensive Care Med 35:698–706CrossRefPubMedGoogle Scholar
  86. 86.
    Honore PM, De Waele E, Jacobs R, Mattens S, Rose T, Joannes-Boyau O, De Regt J, Verfaillie L, Van Gorp V, Boer W, Collin V, Spapen HD (2013) Nutritional and metabolic alterations during continuous renal replacement therapy. Blood Purif 35:279–284CrossRefPubMedGoogle Scholar
  87. 87.
    Pasko DA, Churchwell MD, Btaiche IF, Jain JC, Mueller BA, Renal Replacement Therapy Kinetics Study Group (2009) Continuous venovenous hemodiafiltration trace element clearance in pediatric patients: a case series. Pediatr Nephrol 24:807–813CrossRefPubMedGoogle Scholar
  88. 88.
    Churchwell MD, Pasko DA, Btaiche IF, Jain JC, Mueller BA (2007) Trace element removal during in vitro and in vivo continuous haemodialysis. Nephrol Dial Transplant 22:2970–2977CrossRefPubMedGoogle Scholar
  89. 89.
    Martinez JL, Riera JASI, Jimenez FJJ (2011) Guidelines for specialized nutritional and metabolic support in the critically-ill patient. Update. Consensus SEMICYUC-SENPE: acute renal failure. Nutr Hosp 26:21–26Google Scholar
  90. 90.
    Kliegman RM, BMD S, St Geme J, Schnor NF (eds) (2016) Nelson’s textbook of pediatrics. Saunders Elsevier, PhiladelphiaGoogle Scholar
  91. 91.
    Weinstein M, Babyn P, Zlotkin S (2001) An orange a day keeps the doctor away: scurvy in the year 2000. Pediatrics 108:E55CrossRefPubMedGoogle Scholar
  92. 92.
    Hotz C, Brown KH (2001) Identifying populations at risk of zinc deficiency: the use of supplementation trials. Nutr Rev 59:80–84CrossRefPubMedGoogle Scholar
  93. 93.
    Vinton NE, Dahlstrom KA, Strobel CT, Ament ME (1987) Macrocytosis and pseudoalbinism—manifestations of selenium deficiency. J Pediatr 111:711–717CrossRefPubMedGoogle Scholar

Copyright information

© IPNA 2017

Authors and Affiliations

  1. 1.Stead Family Department of Pediatrics, Division of Nephrology, Dialysis & TransplantationUniversity of Iowa Stead Family Children’s HospitalIowa CityUSA
  2. 2.Stead Family Department of PediatricsUniversity of Iowa Hospitals and ClinicsIowa CityUSA

Personalised recommendations