Growth and growth hormone – Insulin like growth factor – I (GH-IGF-I) axis in chronic anemias

Acta Biomedica

Volumn 88, Issue 1, 2017, Pages 101-111

  Soliman, Ashraf T ^a   De Sanctis, Vincenzo ^b   Yassin, Mohamed ^c   Adel, Ashraf ^d  

^a ALEXANDRIA UNIVERSITY   (Egypt)

^b Pediatric and Adolescent Outpatient Clinic   (Italy)

^c HAMAD MEDICAL CORPORATION   (Qatar)

^d HAMAD GENERAL HOSPITAL   (Qatar)

Author keywords

Growth; Growth hormone (GH); Height (Ht); Height standard deviation score (HtSDS); Insulin like growth factor I (IGF I); Iron; Iron deficiency anemia (IDA); Sickle cell disease; Thalassemia

Indexed keywords

GROWTH HORMONE; SOMATOMEDIN C; HUMAN GROWTH HORMONE; IRON;

ANEMIA; ARTICLE; COGNITION; GONADOTROPIN RELEASE; GROWTH DISORDER; GROWTH RETARDATION; HEIGHT; HUMAN; IRON DEFICIENCY ANEMIA; MOTOR ACTIVITY; SICKLE CELL ANEMIA; THALASSEMIA; ANIMAL; BLOOD; CHILD DEVELOPMENT; COMPLICATION; DIETARY SUPPLEMENT; FEMALE; INFANT; LOW BIRTH WEIGHT; PREGNANCY; PREGNANCY COMPLICATION;

ANEMIA, IRON-DEFICIENCY; ANEMIA, SICKLE CELL; ANIMALS; CHILD DEVELOPMENT; DIETARY SUPPLEMENTS; FEMALE; HUMAN GROWTH HORMONE; HUMANS; INFANT; INFANT, LOW BIRTH WEIGHT; INSULIN-LIKE GROWTH FACTOR I; IRON; PREGNANCY; PREGNANCY COMPLICATIONS, HEMATOLOGIC; THALASSEMIA;

EID: 85020027136     PISSN: 03924203     EISSN: None     Source Type: Journal    
DOI: 10.23750/abm.v88i1.5744     Document Type: Article

References (99)

1. United Nations Children’s Fund, United Nations University, World Health Organization. Iron deficiency anaemia assessment, prevention, and control: a guide for programme managers. Geneva: World Health Organization; 2001 (WHO/ NHD/01.3; http://www.who.int/nutrition/publications/en/ ida_assessment_prevention_control.pdf, accessed 7 May 2015).
2. Stoltzfus RJ, Mullany L, Black RE. Iron deficiency anaemia. In: Ezzati M, Lopez Ad, Rodgers A, Murray CJL, editors. Comparative quantification of health risks: global and regional burden of disease attributable to selected major risk factors. Geneva: World Health Organization; 2004: 163-210 (http://www.who.int/publications/cra/chapters/volume1/0163-0210.pdf?ua=1; accessed 20 May 2015).
3. Balarajan Y, Ramakrishnan U, Ozaltin E, Shankar AH, Subramanian SV. Anaemia in low-income and middle-income countries. Lancet 2011; 378: 2123-2135
4. The global prevalence of anaemia in 2011. WHO Library Cataloguing-in-Publication Data. ISBN 978 92 4 156496 0 (NLM classification: WH 155). http://apps.who.int/iris/bitstream/10665/177094/1/9789241564960_eng.pdf?ua=1&ua=1
5. World Health Organization. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Geneva: World Health Organization; 2011. Available from: (WHO/NMH/NHD/MNM/11.1) http://www.who.int/vmnis/indicators/haemoglobin.
6. Shafir T, Angulo-Barroso R, Calatroni A, Jimenez E, Lozoff B. Effects of iron deficiency in infancy on patterns of motor development over time. Hum Mov Sci 2006; 25: 821-838.
7. Waugh EJ, Polivy J, Ridout R, Hawker GA. A prospective investigation of the relations among cognitive dietary restraint, subclinical ovulatory disturbances, physical activity, and bone mass in healthy young women. Am J Clin Nutr 2007; 86: 1791-801.
8. Rouault TA. The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat Chem Biol 2006; 2: 406-414.
9. Williams TN, Weatherall DJ. World distribution, population genetics, and health burden of the hemoglobinopathies. Cold Spring Harb Perspect Med 2012; 2: a011692.
10. Weatherall DJ. The inherited diseases of hemoglobin are an emerging global health burden. Blood 2010; 115: 4331-4336.
11. http://www.ironhealthalliance.com/disease-states/thalassemia/epidemiology-and-pathophysiology.jsp
12. Soliman AT, elZalabany M, Amer M, Ansari BM. Growth and pubertal development in transfusion-dependent children and adolescents with thalassaemia major and sickle cell disease: a comparative study. J Trop Pediatr 1999; 45: 23-30
13. Rhodes M, Akohoue SA, Shankar SM, Fleming I, Qi An A, Yu C, Acra S, Buchowski MS. Growth Patterns in Children with Sickle Cell Anemia during Puberty. Pediatr Blood Cancer. Pediatr Blood Cancer 2009; 53: 635-641.
14. Esezobor CI, Akintan P, Akinsulie A, Temiye E, Adeyemo T. Wasting and stunting are still prevalent in children with sickle cell anaemia in Lagos, Nigeria. Ital J Pediatr 2016 May 4; 42(1): 45. doi: 10.1186/s13052-016-0257-4.
15. Rouault TA. The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat Chem Biol 2006; 2: 406-414.
16. Galy B, Ferring-Appel D, Sauer SW, Kaden S, Lyoumi S, Puy H, Kölker S, Gröne HJ, Hentze MW. Iron regulatory proteins secure mitochondrial iron sufficiency and function. Cell Metab 2010; 12: 194-201.
17. Zhang DL, Ghosh MC, Rouault TA. The physiological functions of iron regulatory proteins in iron homeostasis – An update. Front Pharmacol 2014; 5: 124. doi: 10.3389/fphar.2014.00124
18. Kohgo Y, Ikuta K, Ohtake T, Torimoto Y, Kato J. Body iron metabolism and pathophysiology of iron overload. Int J Hematol 2008; 88: 7-15.
19. Callahan LS, Thibert KA, Wobken JD, Georgieff MK. Early-life iron deficiency anemia alters the development and long-term expression of parvalbumin and perineuronal nets in the rat hippocampus. Dev Neurosci 2013; 35: 427-436.
20. Hubbard AC, Bandyopadhyay S, Wojczyk BS, Spitalnik SL, Hod EA, Prestia KA. Effect of dietary iron on fetal growth in pregnant mice. Comp Med 2013; 63: 127-135.
21. Guidi GC, Lechi Santonastaso C. Advancements in anemias related to chronic conditions. Clin Chem Lab Med 2010; 48: 1217-1226.
22. Woodall SM, Johnston BM, Breier BH, Gluckman PD. Chronic maternal undernutrition in the rat leads to delayed postnatal growth and elevated blood pressure of offspring. Pediatr Res 1996; 40: 438-443.
23. Allen HL. Anemia and iron deficiency: effects on pregnancy outcome 1,2,3. Am J Clin Nutr. 2000; 71 (Suppl. 5): 1280s-1284s.
24. Murphy JF, O’Riordan J, Newcombe RG, Coles EC, Pearson JF. Relations of hemoglobin levels in first and second trimesters to outcome of pregnancy. Lancet 1986; 1: 992-995.
25. Steer P, Alam MA, Wadsworth J, Welch A. Relation between maternal hemoglobin concentration and birth weight in different ethnic groups. BMJ 1995; 310: 489-491.
26. Kumar KJ, Asha N, Murthy DS, Sujatha M, Manjunath V. Maternal Anemia in Various Trimesters and its Effect on Newborn Weight and Maturity: An Observational Study. Int J Prev Med 2013; 4: 193-199.
27. Moghaddam Tabrizi F, Barjasteh S. Maternal Hemoglobin Levels during Pregnancy and their Association with Birth Weight of Neonates. Iran J Pediatr Hematol Oncol 2015; 5: 211-217.
28. Kalaivani K. Prevalence and consequences of anaemia in pregnancy. Indian J Med Res 2009; 130: 627-633.
29. Wang J, Ren AG, Ye RW, Zheng JC, Li S, Liu JM, Yang RL, Zhang FR, Zhang T, Zhang JB, Li Z. Study on the third trimester hemoglobin concentrations and the risk of low birth weight and preterm delivery. Zhonghua Liu Xing Bing Xue Za Zhi. 2007;28:15-18.
30. Yip R. Significance of an abnormally low or high hemoglobin concentration during pregnancy: special consideration of iron nutrition. Am J Clin Nutr 2000; 72: 272s-279s.
31. Dreyfuss M. Anemia and iron deficiency during pregnancy: etiologies and effects on birth outcomes in Nepal. PhD dissertation. Johns Hopkins University, Baltimore, 1998.
32. Sichieri R, Fonseca VM, Hoffman D, Trugo NM, Moura AS. Lack of association between iron status at birth and growth of preterm infants. Rev Saude Publica 2006; 40: 641-647.
33. Angeles IT, Schultink WJ, Matulssi P, Gross R, Sastroamidjoj S. Increased rate of stunting among anaemic Indonesian pre-school children through iron supplementation. Am J Clin Nutr 1993; 58: 339-342.
34. Chowang L, Soemantri AG, Pollitt E. Iron supplementation and physical growth or rural Indonsian children. Am J Clin Nutr 1988; 47: 496-501.
35. Beard JL. Iron biology in immune function, muscle metabolism and neuronal functioning. J Nutr 2001; 131: 568S-579S.
36. Bhatia D, Seshadri S. Growth performance in anemia and following iron supplementation. Indian Pediatr 1993; 30: 195-200.
37. Soliman AT, Al Dabbagh MM, Habboub AH, Adel A, Humaidy NA, Abushahin A. Linear growth in children with iron deficiency anemia before and after treatment. J Trop Pediatr 2009; 55: 324-327.
38. Bandhu R, Shankar N, Tandon OP. Effect of iron on growth in iron deficient anemic school going children. Indian J Physiol Pharmacol 2003; 47: 59-66.
39. Sachdev H, Gera T, Nestel P. Effect of iron supplementation on physical growth in children: Systematic review of randomized controlled trials. Public Health Nutr 2006; 9: 904-920.
40. Ramakrishnan U, Aburto N, McCabe G, Martorell R. Multimicronutrient interventions but not vitamin a or iron interventions alone improve child growth: Results of 3 meta-analyses. J Nutr 2004; 134: 2592-602.
41. Vucic V, Berti C, Vollhardt C, Fekete K, Cetin I, Koletzko B, Gurinovic M, van’t Veer P. Effect of iron intervention on growth during gestation, infancy, childhood, and adolescence: A systematic review with meta-analysis. Nutr Rev 2013; 71: 386-401.
42. Cardoso MA, Augusto RA, Bortolini GA, Oliveira CS, Tietzman DC, Sequeira LA, Hadler MC, Peixoto Mdo R, Muniz PT, Vitolo MR, Lira PI, Jaime PC; ENFAC Working Group. Effect of Providing Multiple Micronutrients in Powder through Primary Healthcare on Anemia in Young Brazilian Children: A Multicentre Pragmatic Controlled Trial. PLoS One 2016 Mar 14; 11(3): e0151097. doi: 10.1371/journal.pone.0151097.
43. Gera T, Sachdev HP, Nestel P. Effect of iron supplementation on physical performance in children and adolescents: systematic review of randomized controlled trials. Indian Pediatr 2007; 44: 15-24.
44. Chhagan MK, Van den Broeck J, Luabeya KK, Mpontshane N, Tomkins A, Bennish ML. Effect on longitudinal growth and anemia of zinc or multiple micronutrients added to vitamin A: a randomized controlled trial in children aged 6-24 months. BMC Public Health 2010 Mar 18; 10: 145. doi: 10.1186/1471-2458-10-145.
45. Preedy VR, Smith DM, Sugden PH. The effects of 6 hours of hypoxia on protein synthesis in rat tissues in vivo and in vitro. Biochem J 1985; 228: 179-185.
46. Tsunawaki T, Sakai K, Momomura M, Wachi Y, Matsuzawa Y, Iwashita M. Hypoxia alters phosphorylation status of insulin-like growth factor (IGF)-binding protein-1 and attenuates biological activities of IGF-I in HepG2 cell cultures. J Obstet Gynaecol Res 2013; 39: 1367-1373.
47. Kajimura S, Aida K, Duan C. Insulin-like growth factor-binding protein-1 (IGFBP-1) mediates hypoxia-induced embryonic growth and developmental retardation. Proc Natl Acad Sci 2005; 102: 1240-1245.
48. Storch S, Kübler B, Höning S, Ackmann M, Zapf J, Blum W, et al. Transferrin binds insulin-like growth factors and affects binding properties of insulin-like growth factor binding protein-3. FEBS Lett 2001; 509: 395-398.
49. Vakili H, Jin Y, Cattini PA. Negative Regulation of Human Growth Hormone Gene Expression by Insulin Is Dependent on Hypoxia-inducible Factor Binding in Primary Non-tumor Pituitary Cells. The J Biol Chem 2012; 287: 33282-33292. Epub 2012 Jul 25.
50. Ceppi A, Blum JW. Effects of growth hormone on growth performance, haematology, metabolites and hormones in iron-deficient veal calves. Zentralbl Veterinarmed A 1994; 41: 443-458.
51. Blum JW, Hammon H. Endocrine and metabolic aspects in milk-fed calves. Domest Anim Endocrinol 1999; 17: 219-230.
52. Katsumata S, Katsumata-Tsuboi R, Uehara M, Suzuki K. Severe iron deficiency decreases both bone formation and bone resorption in rats. J Nutr 2009; 139: 238-243.
53. Medeiros DM, Stoecker B, Plattner A, Jennings D, Haub M. Iron deficiency negatively affects vertebrae and femurs of rats independently of energy intake and body weight. J Nutr 2004; 134: 3061-3067.
54. Katsumata S, Tsuboi R, Uehara M, Suzuki K. Dietary iron deficiency decreases serum osteocalcin concentration and bone mineral density in rats. Biosci Biotechnol Biochem 2006; 70: 2547-2550.
55. Tran PV, Fretham SJ, Wobken J, Miller BS, Georgieff MK. Gestational-neonatal iron deficiency suppresses and iron treatment reactivates IGF signaling in developing rat hippocampus. Am J Physiol Endocrinol Metab 2012; 302: E316-324.
56. Isguven P, Arslanoglu I, Erol M, Yildiz M, Adal E, Erguven M. Serum levels of ghrelin, leptin, IGF-I, IGFBP-3, insulin, thyroid hormones and cortisol in prepubertal children with iron deficiency. Endocr J 2007; 54: 985-990.
57. Soliman AT, Eldabbagh M, Adel A, Sabt A. Linear growth and circulating IGF-I concentrations in children with Iron deficiency anemia after treatment. Arch Dis Child 2012; 97: A220.
58. Choi JW, Kim SK. Association of serum insulin-like growth factor-I and erythropoiesis in relation to body iron status. Ann Clin Lab Sci 2004; 34: 324-328.
59. Succurro E, Arturi F, Caruso V, Rudi S, Sciacqua A, Andreozzi F, et al. Low insulin-like growth factor-1 levels are associated with anaemia in adult non-diabetic subjects. Thromb Haemost 201; 105: 365-370.
60. De Sanctis V, Soliman AT, Elsedfy H, Skordis N, Kattamis C, Angastiniotis M, et al. Growth and endocrine disorders in thalassemia: The international network on endocrine complications in thalassemia (I-CET) position statement and guidelines. Indian J Endocrinol Metab 2013; 17: 8-18.
61. De Sanctis V, Katz M, Vullo C, Bagni B, Ughi M, Wonke B. Effect of different treatment regimes on linear growth and final height in beta-thalassaemia major. Clin Endocrinol (Oxf) 1994; 40: 791-798.
62. De Sanctis V. Growth and puberty and its management in thalassaemia. Horm Res 2002; 58 (Suppl 1): 72-79.
63. Kyriakou A, Skordis N. Thalassaemia and aberrations of growth and puberty. Mediterr J Hematol Infect Dis 2009 Jul 27; 1(1): e2009003. doi: 10.4084/MJHID.2009.003.
64. Soliman AT, Abushahin A, Abohezeima K, Khalafallah H, Adel A, Elawwa A, et al. Age related IGF-I changes and IGF-I generation in thalassemia major. Pediatr Endocrinol Rev 2011; 8 (Suppl 2): 278-283.
65. Soliman AT, Khalafallah H, Ashour R. Growth and factors affecting it in thalassemia major. Hemoglobin 2009; 33 (Suppl 1): S116-126.
66. Soliman AT, El Banna N, Ansari BM. GH response to provocationand circulating IGF-I and IGF-binding protein-3 concentrations, the IGF-I generation test and clinical response to GH therapy in children with beta-thalassaemia. Eur J Endocrinol 1998; 138: 394-400.
67. Soliman AT, El Banna N, Abdel Fattah M, ElZalabani MM, Ansari BM. Bone mineral density in prepubertal children with beta-thalassemia: Correlation with growth and hormonal data. Metabolism 1998; 47: 541-548.
68. Soliman AT, elZalabany MM, Mazloum Y, Bedair SM, Ragab MS, Rogol AD, Ansari BM. Spontaneous and provoked growth hormone (GH) secretion and insulin-like growth factor I (IGF-I) concentration in patients with beta thalassaemia and delayed growth. J Trop Pediatr 1999; 45: 327-337.
69. Soliman A, De Sanctis V, Elsedfy H, Yassin M, Skordis N, Karimi M, et al. Growth hormone deficiency in adults with thalassemia: An overview and the I-CET recommendations. Georgian Med News 2013; 79-88.
70. Soliman AT, El-Matary W, Fattah MM, Nasr IS, El Alaily RK, Thabet MA. The effect of high-calorie diet on nutritional parameters of children with beta-thalassaemia major. Clin Nutr 2004; 23: 1153-1158.
71. Bennett EL. Understanding growth failure in children with homozygous sickle-cell disease. J Pediatr Oncol Nurs 2011; 28: 67-74.
72. Soliman AT, elZalabany M, Amer M, Ansari BM. Growth and pubertal development in transfusion-dependent children and adolescents with thalassaemia major and sickle cell disease: a comparative study. J Trop Pediatr 1999; 45: 23-30.
73. Henderson RA, Saavedra JM, Dover GJ. Prevalence of impaired growth in children with homozygous sickle cell anemia. Am J Med Sci 1994; 307: 405-407.
74. Zemel BS, Kawchak DA, Ohene-Frempong K, Schall JI, Stallings VA. Effects of delayed pubertal development, nutritional status, and disease severity on longitudinal patterns of growth failure in children with sickle cell disease. Pediatr Res 2007; 61: 607-613.
75. Singhal A, Thomas P, Cook R, Wierenga K, Serjeant G Delayed adolescent growth in homozygous sickle cell disease. Arch Dis Child 1994; 71: 404–408.
76. Olambiwonnu NO, Penny R, Frasier SD. Sexual maturation in subjects with sickle cell anemia: studies of serum gonadotropin concentration, height, weight and skeletal age. J Pediatr 1975; 87: 459-464.
77. Platt OS, Rosenstock W, Espeland MA.Influence of sickle hemoglobinopathies on growth and development. N Engl J Med 1984; 311: 7-12.
78. Stevens MC, Maude GH, Cupidore L, Jackson H, Hayes RJ, Serjeant GR Prepubertal growth and skeletal maturation in children with sickle cell disease. Pediatrics 1986; 78: 124-132.
79. Wang WC, Morales KH, Scher CD, Styles L, Olivieri N, Adams R, Brambilla D. Effect of long-term transfusion on growth in children with sickle cell anemia: results of the STOP trial. J Pediatr 2005; 147: 244-247.
80. Soliman AT, el Banna N, alSalmi I, De Silva V, Craig A, Asfour M. Growth hormone secretion and circulating insulin-like growth factor-I (IGF-I) and IGF binding protein-3 concentrations in children with sickle cell disease. Metabolism 1997; 46: 1241-1245.
81. Soliman AT, Darwish A, Mohammed SH, Bassiony MR, el Banna N, Asfour M. Circulating growth hormone (GH), insulin-like growth factor-I (IGF-I) and free thyroxine, GH response to clonidine provocation and CT scanning of the hypothalamic-pituitary area in children with sickle cell disease. J Trop Pediatr 1995; 41: 285-289.
82. Collett-Solberg PF, Fleenor D, Schultz WH, Ware RE. Short stature in children with sickle cell anemia correlates with alterations in the IGF-I axis. J Pediatr Endocrinol Metab 2007; 20: 211-218.
83. Nunlee-Bland G, Rana SR, Houston-Yu PE, Odonkor W. Growth hormone deficiency in patients with sickle cell disease and growth failure. J Pediatr Endocrinol Metab 2004; 17: 601-606.
84. Smiley D, Dagogo-Jack S, Umpierrez G. Therapy insight: Metabolic and endocrine disorders in sickle cell disease. Nat Clin Pract Endocrinol Metab 2008 Feb; 4(2): 102-9. doi: 10.1038/ncpendmet0702
85. Luporini SM, Bendit I, Manhani R, Bracco OL, Manzella L, Giannella-Neto D. Growth hormone and insulin-like growth factor I axis and growth of children with different sickle cell anemia haplotypes. J Pediatr Hematol Oncol 2001; 23: 357-363.
86. Filho IL, Leite AC, Moura PG, Ribeiro GS, Cavalcante AC, Azevedo FC, Andrada-Serpa MJ. Genetic polymorphisms and cerebrovascular disease in children with sickle cell anemia from Rio de Janeiro. Brazil. Arq Neuropsiquiatr 2011; 69: 431-435.
87. Olambiwonnu NO, Penny R, Frasier SD. Sexual maturation in subjects with sickle cell anemia: studies of serum gonadotropin concentration, height, weight and skeletal age. J Pediatr 1975; 87: 459-464.
88. Singhal A, Gabay L, Serjeant GR. Testosterone deficiency and extreme retardation of puberty in homozygous sickle-cell disease. West Indian Med J 1995; 44: 20-23.
89. Badaloo A, Jackson AA, Jahoor F. Whole body protein turnover and resting metabolic rate in homozygous sickle cell disease. Clin Sci 1989; 77: 93-97.
90. Borel MJ, Buchowski MS, Turner EA, Peeler BB, Goldstein RE, Flakoll PJ. Alterations in basal nutrient metabolism increase resting energy expenditure in sickle cell disease. Am J Physiol 1998; 274: E357-E364.
91. Barden EM, Zemel BS, Kawchak DA, Goran MI, Ohene-Frempong K, Stallings VA. Total and resting energy expenditure in children with sickle cell disease. J Pediatr 2000; 136: 73-79.
92. Nelson MC, Zemel BS, Kawchak DA, Barden EM, Frongillo EA, Coburn SP, Ohene-Frempong K, Stallings VA. Vitamin B6 status of children with sickle cell disease. J Pediatr Hematol Oncol 2002; 24: 463-469.
93. Buison AM, Kawchak DA, Schall J, Ohene-Frempong K, Stallings VA, Zemel BS. Low vitamin D status in children with sickle cell disease. J Pediatr 2004; 145: 622–627.
94. Natta C, Machlin L. Plasma levels of tocopherol in sickle cell anemia subjects. Am J Clin Nutr 1979; 32: 1359-1362.
95. Natta CL, Machlin LJ, Brin M. A decrease in irreversibly sickled erythrocytes in sickle cell anemia patients given vitamin E. Am J Clin Nutr 1980; 33: 968-971.
96. Schall JI, Zemel BS, Kawchak DA, Ohene-Frempong K, Stallings VA. Vitamin A status, hospitalizations, and other outcomes in young children with sickle cell disease. J Pediatr 2004; 145: 99-106.
97. Leonard MB, Zemel BS, Kawchak DA, Ohene-Frempong K, Stallings VA. Plasma zinc status, growth, and maturation in children with sickle cell disease. J Pediatr 1998; 132: 467-471.
98. Zemel BS, Kawchak DA, Fung EB, Ohene-Frempong K, Stallings VA. Effect of zinc supplementation on growth and body composition in children with sickle cell disease. Am J Clin Nutr 2002; 75: 300-307.
99. Phebus CK, Maciak BJ, Gloninger MF, Paul HS. Zinc status of children with sickle cell disease: relationship to poor growth. Am J Hematol 1988; 29: 67-73.