Higher levels of s-RANKL and osteoprotegerin in children and adolescents with type 1 diabetes mellitus may indicate increased osteoclast signaling and predisposition to lower bone mass: a multivariate cross-sectional analysis

Osteoporosis International

Volumn 27, Issue 4, 2016, Pages 1631-1643

  Tsentidis, C ^a   Gourgiotis, D ^a   Kossiva, L ^a   Doulgeraki, A ^b   Marmarinos, A ^a   Galli Tsinopoulou, A ^c   Karavanaki, K ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b AGHIA SOPHIA CHILDREN S HOSPITAL   (Greece)

^c ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

Author keywords

Bone metabolism; Multivariate analysis; Osteoporosis; Osteoprotegerin; s RANKL; Type 1 diabetes

Indexed keywords

25 HYDROXYVITAMIN D; CARBOXY TERMINAL TELOPEPTIDE; ELECTROLYTE; MAGNESIUM; OSTEOCALCIN; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PARATHYROID HORMONE; SOMATOMEDIN C; BIOLOGICAL MARKER; TNFSF11 PROTEIN, HUMAN;

ADOLESCENT; ARTICLE; BONE DENSITY; BONE MASS; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE PREDISPOSITION; DUAL ENERGY X RAY ABSORPTIOMETRY; FEMALE; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; LUMBAR SPINE; MALE; MULTIVARIATE ANALYSIS; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; RISK FACTOR; SIGNAL TRANSDUCTION; BLOOD; BONE DISEASES, METABOLIC; BONE REMODELING; CASE CONTROL STUDY; CHILD; COMPLICATION; LUMBAR VERTEBRA; OSTEOPOROSIS; PATHOPHYSIOLOGY; PHOTON ABSORPTIOMETRY; PHYSIOLOGY; PROCEDURES;

ABSORPTIOMETRY, PHOTON; ADOLESCENT; BIOMARKERS; BONE DENSITY; BONE DISEASES, METABOLIC; BONE REMODELING; CASE-CONTROL STUDIES; CHILD; CROSS-SECTIONAL STUDIES; DIABETES MELLITUS, TYPE 1; FEMALE; HUMANS; LUMBAR VERTEBRAE; MALE; OSTEOCLASTS; OSTEOPOROSIS; OSTEOPROTEGERIN; RANK LIGAND; SIGNAL TRANSDUCTION;

EID: 84961053607     PISSN: 0937941X     EISSN: 14332965     Source Type: Journal    
DOI: 10.1007/s00198-015-3422-5     Document Type: Article

References (49)

1. (2013) IDF Diabetes Atlas. International Diabetes Federation
2. Schwartz AV, Sellmeyer DE (2007) Diabetes fracture and bone fragility. Curr Osteoporos Rep 5:105–111
3. Sealand R, Razavi C, Adler RA (2013) Diabetes mellitus and osteoporosis. Curr Diabetes Rep 13:411–418
4. Jackuliak P, Payer J (2014) Osteoporosis, fractures, and diabetes. Int J Endocrinol 2014:820615
5. Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes—a meta-analysis. Osteoporos Int: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 18:427–444
6. Rakel A, Sheehy O, Rahme E, LeLorier J (2008) Osteoporosis among patients with type 1 and type 2 diabetes. Diabetes Metab 34:193–205
7. Strotmeyer ES, Cauley JA (2007) Diabetes mellitus bone mineral density and fracture risk. Curr Opin Endocrinol Diabetes Obes 14:429–435
8. Salerno M, Argenziano A, Di Maio S, Gasparini N, Formicola S, De Filippo G, Tenore A (1997) Pubertal growth, sexual maturation, and final height in children with IDDM. Effects of age at onset and metabolic control. Diabetes Care 20:721–724
9. Ahmed M, Connors M, Drayer N, Jones J, Dunger D (1998) Pubertal growth in IDDM is determined by HbA1c levels, sex, and bone age. Diabetes Care 21:831–835
10. Thrailkill KM, Lumpkin CKJ, Bunn RC, Kemp SF, Fowlkes JL (2005) Is insulin an anabolic agent in bone? Dissecting the diabetic bone for clues. Am J Physiol Endocrinol Metab 289:E735–E745
11. Merlotti D, Gennari L, Dotta F, Lauro D, Nuti R (2010) Mechanisms of impaired bone strength in type 1 and 2 diabetes. Nutr Metab Cardiovasc Dis 20:683–690
12. Dhaon P, Shah VN (2014) Type 1 diabetes and osteoporosis: a review of literature. Indian J Endocrinol Metab 18:159–165
13. Starup-Linde J, Eriksen SA, Lykkeboe S, Handberg A, Vestergaard P (2014) Biochemical markers of bone turnover in diabetes patients—a meta-analysis, and a methodological study on the effects of glucose on bone markers. Osteoporos Int: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 25:1697–1708
14. Kearns AE, Khosla S, Kostenuik PJ (2008) Receptor activator of nuclear factor kappaB ligand and osteoprotegerin regulation of bone remodeling in health and disease. Endocr Rev 29:155–192
15. Loureiro MB, Ururahy MA, Freire-Neto FP et al (2014) Low bone mineral density is associated to poor glycemic control and increased OPG expression in children and adolescents with type 1 diabetes. Diabetes Res Clin Pract 103:452–457
16. Galluzzi F, Stagi S, Salti R, Toni S, Piscitelli E, Simonini G, Falcini F, Chiarelli F (2005) Osteoprotegerin serum levels in children with type 1 diabetes: a potential modulating role in bone status. Eur J Endocrinol / Eur Fed Endocr Soc 153:879–885
17. Abd El Dayem S, El-Shehaby A, Abd El Gafar A, Fawzy A, Salama H (2011) Bone density, body composition, and markers of bone remodeling in type 1 diabetic patients. Scand J Clin Lab Invest 71:387–393
18. Lambrinoudaki I, Tsouvalas E, Vakaki M, Kaparos G, Stamatelopoulos K, Augoulea A, Pliatsika P, Alexandrou A, Creatsa M, Karavanaki K (2013) Osteoprotegerin, Soluble Receptor Activator of Nuclear Factor- kappa B Ligand, and Subclinical Atherosclerosis in Children and Adolescents with Type 1 Diabetes Mellitus. Int J Endocrinol 2013:102120
19. Tsentidis C, Gourgiotis D, Kossiva L, Marmarinos A, Doulgeraki A, Karavanaki K (2015) Sclerostin distribution in children and adolescents with type 1 diabetes mellitus and correlation with bone metabolism and bone mineral density. Pediatr Diabetes. doi:10.1111/pedi.12288
20. Magkos F, Manios Y, Babaroutsi E, Sidossis LS (2006) Development and validation of a food frequency questionnaire for assessing dietary calcium intake in the general population. Osteoporos Int: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 17:304–312
21. Avgerinos A, Argiropoulou EC, Almond L, Michalopoulou M (2000) A new instrument for evaluating energy expenditure: convergent validity and reliability of the physical activity and lifestyle questionnaire (PALQ). Sport Perform Health 4:281–300
22. Gunczler P, Lanes IR, Paolil M, Martinis R, Villaroel O, Weisinger JR (2001) Decreased bone mineral density and bone formation markers shortly after diagnosis of clinical type 1 diabetes mellitus. J Pediatr Endocrinol Metab 14:525–528
23. Valerio G, del Puente A, Esposito-del Puente A, Buono P, Mozzillo E, Franzese A (2002) The lumbar bone mineral density is affected by long-term poor metabolic control in adolescents with type 1 diabetes mellitus. Horm Res 58:266–272
24. Camurdan MO, Ciaz P, Bideci A, Demirel F (2007) Role of hemoglobin A(1c), duration and puberty on bone mineral density in diabetic children. Pediatr Int: Off J Japan Pediatr Soc 49:645–651
25. Hamed EA, Faddan NH, Elhafeez HA, Sayed D (2011) Parathormone–25(OH)-vitamin D axis and bone status in children and adolescents with type 1 diabetes mellitus. Pediatr Diabetes 12:536–546
26. Moyer-Mileur L, Slater H, Jordan K, Murray M (2008) IGF-1 and IGF-binding proteins and bone mass, geometry, and strength: relation to metabolic control in adolescent girls with type 1 diabetes. J Bone Miner Res 23:1884–1891
27. Maggio ABR, Ferrari S, Kraenzlin M, Marchand LM, Schwitzgebel V, Beghetti M, Rizzoli R, Farpour-Lambert NJ (2010) Decreased bone turnover in children and adolescents with well controlled type 1 diabetes. J Pediatr Endocrinol Metab 23:697–707
28. AboElAsrar M, Elbarbary N, Elshennawy D, Omar A (2012) Insulin-like growth factor-1 cytokines cross-talk in type 1 diabetes mellitus: relationship to microvascular complications and bone mineral density. Cytokine 59:86–93
29. Heap J, Murray MA, Miller SC, Jalili T, Moyer-Mileur LJ (2004) Alterations in bone characteristics associated with glycemic control in adolescents with type 1 diabetes mellitus. J Pediatr 144:56–62
30. Mastrandrea LD, Wactawski-Wende J, Donahue RP, Hovey KM, Clark A, Quattrin T (2008) Young women with type 1 diabetes have lower bone mineral density that persists over time. Diabetes Care 31:1729–1735
31. Ersoy B, Gökşen D, Darcan S, Mavi E, Oztürk C (1999) Evaluation of bone mineral density in children with diabetes mellitus. Indian J Pediatr 66:375–379
32. Saha MT, Sievanen H, Salo MK, Tulokas S, Saha HH (2009) Bone mass and structure in adolescents with type 1 diabetes compared to healthy peers. Osteoporos Int: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 20:1401–1406
33. Moyer-Mileur LJ, Dixon SB, Quick JL, Askew EW, Murray MA (2004) Bone mineral acquisition in adolescents with type 1 diabetes. J Pediatr 145:662–669
34. Brandao FR, Vicente EJ, Daltro CH, Sacramento M, Moreira A, Adan L (2007) Bone metabolism is linked to disease duration and metabolic control in type 1 diabetes mellitus. Diabetes Res Clin Pract 78:334–339
35. Karagüzel G, Akçurin S, Ozdem S, Boz A, Bircan I (2006) Bone mineral density and alterations of bone metabolism in children and adolescents with type 1 diabetes mellitus. J Pediatr Endocrinol Metab 19:805–814
36. Aboelasrar M, Farid S, El Maraghy M, Mohamedeen A (2010) Serum osteocalcin, zinc nutritive status and bone turnover in children and adolescents with type1 diabetes mellitus. Pediatr Diabetes 11:35–113
37. Pater A, Sypniewska G, Pilecki O (2010) Biochemical markers of bone cell activity in children with type 1 diabetes mellitus. J Pediatr Endocrinol Metab 23:81–86
38. Xiang GD, Sun HL, Zhao LS (2007) Changes of osteoprotegerin before and after insulin therapy in type 1 diabetic patients. Diabetes Res Clin Pract 76:199–206
39. Van Sickle B, Simmons J, Hall R, Raines M, Ness K, Spagnoli A (2009) Increased circulating IL-8 is associated with reduced IGF-1 and related to poor metabolic control in adolescents with type 1 diabetes mellitus. Cytokine 48:290–294
40. Ekstrom K, Salemyr J, Zachrisson I, Carlsson-Skwirut C, Ortqvist E, Bang P (2007) Normalization of the IGF-IGFBP axis by sustained nightly insulinization in type 1 diabetes. Diabetes Care 30:1357–1363
41. Rubin J, Ackert-Bicknell CL, Zhu L, Fan X, Murphy TC, Nanes MS, Marcus R, Holloway L, Beamer WG, Rosen CJ (2002) IGF-I regulates osteoprotegerin (OPG) and receptor activator of nuclear factor-kappaB ligand in vitro and OPG in vivo. J Clin Endocrinol Metab 87:4273–4279
42. Pascual J, Argente J, Lopez M, Muñoz M, Martinez G, Vazquez M, Jodar E, Perez-Cano R, Hawkins F (1998) Bone mineral density in children and adolescents with diabetes mellitus type 1 of recent onset. Calcif Tissue Int 62:31–35
43. De Schepper J, Smitz J, Rosseneu S, Bollen P, Louis O (1998) Lumbar spine bone mineral density in diabetic children with recent onset. Horm Res 50:193–196
44. Vázquez Gámez MÁ, Marín Pérez JM, Montoya García MJ, Moruno García RM, Argüelles Martín F, Pérez Cano R (2008) Evolución de la masa ósea durante la infancia y adolescencia en niños con diabetes mellitus tipo 1. Med Clin (Barc) 130:526–530
45. Liu EY, Wactawski-Wende J, Donahue RP, Dmochowski J, Hovey K, Quattrin T (2003) Does low bone mineral density start in post-teenage years in women with type 1 diabetes? Diabetes Care 26:2365–2369
46. Onder A, Cetinkaya S, Tunc O, Aycan Z (2013) Evaluation of bone mineral density in children with type 1 diabetes mellitus. J Pediatr Endocrinol Metab 26:1077–1081
47. Salvatoni A, Mancassola G, Biasoli R, Cardani R, Salvatore S, Broggini M, Nespoli L (2004) Bone mineral density in diabetic children and adolescents: a follow-up study. Bone 34:900–904
48. Heilman K, Zilmer M, Zilmer K, Tillmann V (2009) Lower bone mineral density in children with type 1 diabetes is associated with poor glycemic control and higher serum ICAM-1 and urinary isoprostane levels. J Bone Miner Metab 27:598–604
49. Roma-Giannikou E, Adamidis D, Gianniou M, Nikolara R, Matsaniotis N (1997) Nutritional survey in Greek children: nutrient intake. Eur J Clin Nutr 51:273–285