Bone turnover markers and bone mineral density in prepubertal obese children
Bone health in prepubertal childhood obesity
Keywords:
procollagen type I N-terminal propeptide; C-terminal collagen type I extension propeptide; dual-energy radiograph absorptiometry; obesity; prepubertal
Abstract
Background Growing evidence suggests that childhood obesity has an impact on bone metabolism. Its entails of bone resorption, destruction of mature mineralized bone by osteoclasts followed by ossification, bone formation by osteoblasts, to maintain the dynamic nature of bone. Serum C-telopeptide of collagen cross-links (CTX) is considered a bone resorption marker while serum procollagen type I N-propeptide (PINP) is considered abone formation marker. Previous studies have reported the abnormality of these bone turnover marker in obese children.
Objective To compare bone turnover markers and bone mineral density (BMD) in obese prepubertal children to those of normoweight children.
Methods Bone metabolism was evaluated by measuring serum PINP as a bone formation marker and CTX level as a bone resorption marker by enzyme-linked immunosorbent assay. We used dual-energy X-ray absorptiometry (DEXA) scan to evaluate BMD in 60 prepubertal children with obesity and 30 healthy prepubertal normoweight children.
Results The CTX was significantly higher in the case group compared to the control group (P=0.001). The case group also had significantly lower mean BMD (P=0.001) and BMD Z-score (P=0.001). C-telopeptide of collagen cross-links in the case group had significant positive correlations with waist circumference (P=0.001), BMI (P=0.001), and BMI Z-score (P=0.001). Significant negative correlations were found between waist circumference, BMI, and BMI Z-score with procollagen type I N-terminal propeptide, BMD, and BMD Z-score.
Conclusion Obesity has a negative impact on bone health. Low BMD was associated with high CTX in prepubertal obese children.
References
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2. Fintini D, Cianfarani S, Cofini M, Andreoletti A, Ubertini GM, Cappa M, et al. The bones of children with obesity. Front Endocrinol (Lausanne). 2020; 11:200. DOI: https://doi.org/10.3389/fendo.2020.00200
3. Dimitri P. The impact of childhood obesity on skeletal health and development. J Obes Metab Syndr. 2019; 28:4-17. DOI: https://doi.org/10.7570/jomes.2019.28.1.4
4. da Silva VN, Fiorelli LN, da Silva CC, Kurokawa CS, Goldberg TBL. Do metabolic syndrome and its components have an impact on bone mineral density in adolescents? Nutr Metab (Lond). 2017; 14:1. DOI: https://doi.org/10.1186/s12986-016-0156-0
5. Barroso LN, Farias DR, Soares-Mota M, Bettiol H, Barbieri MA, Foss MC, et al. Waist circumference is an effect modifier of the association between bone mineral density and glucose metabolism. Arch Endocrinol Metab. 2018; 62:285-95. DOI: https://doi.org/10.20945/2359-3997000000040
6. Bhattoa HP, Cavalier E, Eastell R, Heijboer AC, Jørgensen NR, Makris K, et al. Analytical considerations and plans to standardize or harmonize assays for the reference bone turnover markers PINP and ?-CTX in blood. Clin Chim Acta. 2021; 515:16-20. DOI: https://doi.org/10.1016/j.cca.2020.12.023
7. Shetty S, Kapoor N, Bondu JD, Thomas N, Paul TV. Bone turnover markers: Emerging tool in the management of osteoporosis. Indian J Endocrinol Metab. 2016; 20:846?52. DOI: https://doi.org/10.4103/2230-8210.192914
8. Macías I, Alcorta-Sevillano N, Rodríguez CI, Infante A. Osteoporosis, and the potential of cell-based therapeutic strategies. Int J Mol Sci. 2020; 21:1653. DOI: https://doi.org/10.3390/ijms21051653
9. Greenblatt MB, Tsai JN, Wein MN. Bone turnover markers in the diagnosis and monitoring of metabolic bone disease. Clin Chem. 2017; 63:464?74. DOI: https://doi.org/10.1373/clinchem.2016.259085
10. Bhattoa HP. Laboratory aspects and clinical utility of bone turnover markers. EJIFCC. 2018; 29:117-28.
11. Sakka SD, Cheung MS. Management of primary and secondary osteoporosis in children. Ther Adv Musculoskelet Dis. 2020; 12:1759720X20969262. DOI: https://doi.org/10.1177/1759720X20969262
12. Bachrach LK, Gordon CM, Section on Endocrinology; Sills IN, Lynch JL, Casella SJ, DiMeglio LA, et al. Bone densitometry in children and adolescents. Pediatrics. 2016;138: e20162398 DOI: https://doi.org/10.1542/peds.2016-2398
13. Diabetes Endocrine Metabolism Pediatric Unit Cairo University Children’s Hospital. Egyptian growth curves: Egyptian growth curve for boys and girls 2-21 years height, weight, and body mass index for age percentile.2008, November,28. Available from http:// dempuegypt.blogspot.com.eg/
14. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 2000; 320:1240-3. DOI: https://doi.org/10.1136/bmj.320.7244.1240
15. Krebs NF, Himes JH, Jacobson D, Nicklas TA, Guilday P, Styne D. Assessment of child and adolescent overweight and obesity. Pediatrics 2007;120: S193-228. DOI: https://doi.org/10.1542/peds.2007-2329D
16. Martinez-Millana A, Hulst JM, Boon M, Witters P, Fernandez-Llatas C, Asseiceira I, et al. Optimisation of children z-score calculation based on new statistical techniques. PLoS One. 2018 Dec 20;13(12): e0208362. doi: 10.1371/journal.pone.0208362. PMID: 30571681; PMCID: PMC6301782.
17. Styne DM, Arslanian SA, Connor EL, Farooqi IS, Murad MH, Silverstein JH, et al. Pediatric obesity-assessment, treatment, and prevention: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2017; 102:709-57. DOI: https://doi.org/10.1210/jc.2016-2573
18. Fernandez GR, Redden DT, Pietrobella A, Allison DB. Waist circumference percentiles in nationally representative samples of African American, European-American, and Mexican American children and adolescents. J Pediatr. 2004; 145:439–44. DOI: https://doi.org/10.1016/j.jpeds.2004.06.044
19. Marshall WA, Tanner JM. Variations in pattern of pubertal changes in girls. Arch Dis Child. 1969 Jun;44(235):291-303. Doi: https://doi.org/10.1136/adc.44.235.291. PMID: 5785179; PMCID: PMC2020314.
20. Pagana KD, Pagana TJ, Pagana TN. Mosby’s Diagnostic & Laboratory Test Reference. 14th ed. St. Louis, Mo: Elsevier; 2019.
21. Marshall WA, Tanner JM. Variations in the pattern of pubertal changes in boys. Arch Dis Child. 1970 Feb;45(239):13-23. DOI: https://doi.org/10.1136/adc.45.239.13. PMID: 5440182; PMCID: PMC2020414.
22. Saber LM, Mahran HN, Baghdadi HH, Al Hawsawi ZM. Interrelationship between bone turnover markers, calciotropic hormones and leptin in obese Saudi children. Eur Rev Med Pharmacol Sci. 2015; 19:4332-43.
23. Grunwald T, Fadia S, Bernstein B, Naliborski M, Wu S, de Luca F. Vitamin D supplementation, the metabolic syndrome, and oxidative stress in obese children. J Pediatr Endocrinol Metabol. 2017; 30:383–8. DOI: https://doi.org/10.1515/jpem-2016-0211
24. Cheng L. The convergence of two epidemics: vitamin D deficiency in obese school-aged children. J Pediatr Nursing. 2018; 38:20–6. DOI: https://doi.org/10.1016/j.pedn.2017.10.005
25. Zakharova I, Klimov L, Kuryaninova V, Nikitina I, Malyavskaya S, Dolbnya S, et al. Vitamin D insufficiency in overweight and obese children and adolescents. Front Endocrinol. 2019; 10:103. DOI: https://doi.org/10.3389/fendo.2019.00103
26. Epsley S, Tadros S, Farid A, Kargilis D, Mehta S, Rajapakse CS. The effect of inflammation on bone. Front Physiol. 2021; 11:511799. DOI: https://doi.org/10.3389/fphys.2020.511799
27. Grace C, Vincent R, Aylwin SJ. High prevalence of vitamin D insufficiency in a United Kingdom urban morbidly obese population: implications for testing and treatment. Surg Obes Relat Dis. 2014; 10:355-60. DOI: https://doi.org/10.1016/j.soard.2013.07.017
28. Grethen E, Hill KM, Jones R, Cacucci BM, Gupta CE, Acton A, et al. Serum leptin, parathyroid hormone, 1,25-dihydroxyvitamin D, fibroblast growth factor 23, bone alkaline phosphatase, and sclerostin relationships in obesity. J Clin Endocrinol Metab. 2012; 97:1655-62. DOI: https://doi.org/10.1210/jc.2011-2280
29. Gajewska J, Ambroszkiewicz J, Klemarczyk W, Che?chowska M, Weker H, Szamotulska K. The effect of weight loss on body composition, serum bone markers, and adipokines in prepubertal obese children after 1-year intervention. Endocr Res. 2018; 43:80-9. DOI: https://doi.org/10.1080/07435800.2017.1403444
30. Roy B, Curtis ME, Fears LS, Nahashon SN, Fentress HM. Molecular mechanisms of obesity-induced osteoporosis and muscle atrophy. Front Physiol. 2016; 7:439. DOI: https://doi.org/10.3389/fphys.2016.00439
31. Souza PPC, Lerner UH. The role of cytokines in inflammatory bone loss. Immunol Invest. 2013; 42:555–622. DOI: https://doi.org/10.3109/08820139.2013.822766
32. Pagnotti GM, Styner M, Uzer G, Patel VS, Wright LE, Ness KK, et al. Combating osteoporosis and obesity with exercise: leveraging cell mechanosensitivity. Nat Rev Endocrinol. 2019; 15:339–55. DOI: https://doi.org/10.1038/s41574-019-0170-1
33. Brunetti G, Papadia F, Tummolo A, Fischetto R, Nicastro F, Piacente L, et al. Impaired bone remodeling in children with osteogenesis imperfecta treated and untreated with bisphosphonates: the role of DKK1, RANKL, and TNF-a. Osteopor Int. 2016;27:2355–65. DOI: https://doi.org/10.1007/s00198-016-3501-2
34. Dimitri P, Wales JK, Bishop N. Adipokines, bone-derived factors and bone turnover in obese children; evidence for altered fat-bone signalling resulting in reduced bone mass. Bone. 2011; 48:189-96. DOI: https://doi.org/10.1016/j.bone.2010.09.034
35. Dimitri P, Jacques RM, Paggiosi M, King D, Walsh J, Taylor ZA, et al. Leptin may play a role in bone microstructural alterations in obese children. J Clin Endocrinol Metab. 2015; 100:594-602. DOI: https://doi.org/10.1210/jc.2014-3199
36. Gállego Suárez C, Singer BH, Gebremariam A, Lee JM, Singer K. The relationship between adiposity and bone density in U.S. children and adolescents. PLoS One. 2017;12:e0181587. DOI: https://doi.org/10.1371/journal.pone.0181587
37. Milyani AA, Kabli YO, Al-Agha AE. The association of extreme body weight with bone mineral density in Saudi children. Ann Afr Med 2022; 21:16-20. DOI: https://doi.org/10.4103/aam.aam_58_20
38. Dimitri P, Wales JK, Bishop N. Fat and bone in children: differential effects of obesity on bone size and mass according to fracture history. J Bone Miner Res. 2010; 25:527-36. DOI: https://doi.org/10.1359/jbmr.090823
39. Viljakainen HT, Valta H, Lipsanen-Nyman M, Saukkonen T, Kajantie E, Andersson S, et al. Bone characteristics and their determinants in adolescents and young adults with early-onset severe obesity. Calcif Tissue Int. 2015; 97:364-75. DOI: https://doi.org/10.1007/s00223-015-0031-4
40. Mughal MZ, Khadilkar AV. The accrual of bone mass during childhood and puberty. Curr Opin Endocrinol Diabetes Obes. 2011; 18:28-32. DOI: https://doi.org/10.1097/MED.0b013e3283416441
41. Lim HS, Byun DW, Suh KI, Park HK, Kim HJ, Kim TH, et al. Is there a difference in serum vitamin D levels and bone mineral density according to body mass index in young adult women? J Bone Metab. 2019; 26:145-50. DOI: https://doi.org/10.11005/jbm.2019.26.3.145
42. Sims NA, Martin TJ. Coupling the activities of bone formation and resorption: a multitude of signals within the basic multicellular unit. Bonekey Rep. 2014; 3:481. DOI: https://doi.org/10.1038/bonekey.2013.215
43. Tournadre A, Vial G, Capel F, Soubrier M, Boirie Y. Sarcopenia. Joint Bone Spine. 2019; 86:309-14. DOI: https://doi.org/10.1016/j.jbspin.2018.08.001
44. Clark EM, Ness AR, Tobias JH. Adipose tissue stimulates bone growth in prepubertal children. J Clin Endocrinol Metabol. 2006; 91:2534–41. DOI: https://doi.org/10.1210/jc.2006-0332
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Published
2024-11-14
How to Cite
1.
Taha O, Elhwary A, Shoeib S, Rashad Y, Ata D. Bone turnover markers and bone mineral density in prepubertal obese children. PI [Internet]. 14Nov.2024 [cited 21Dec.2024];64(6). Available from: https://paediatricaindonesiana.org/index.php/paediatrica-indonesiana/article/view/3632
Section
Pediatric Endocrinology
Copyright (c) 2024 Ola Taha, Amany Elhwary, Sarah M. Shoeib, Yosra Fouad Mohammed Rashad, Dina Ata
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Received 2023-11-07
Accepted 2024-11-14
Published 2024-11-14
Accepted 2024-11-14
Published 2024-11-14
