Implications of Vitamin D Status for Children’s Bone Health: A Data Mining Analyses of Observational Studies

Mariana Leonel Martins; Beatriz Fernandes Arrepia; Lucas Jural; José Vicente-Gomila; Daniele Masterson; Lucianne Cople Maia; Maria Augusta Visconti; Andréa Fonseca-Gonçalves

Authors

Mariana Leonel Martins
Beatriz Fernandes Arrepia
Lucas Jural
José Vicente-Gomila
Daniele Masterson
Lucianne Cople Maia
Maria Augusta Visconti
Andréa Fonseca-Gonçalves

Keywords:

Bibliometrics, Vitamin D, Bone Density, Child

Abstract

Objective: To investigate associations/correlations between bone alterations and vitamin D status in children through data mining analyses based on observational studies. Material and Methods: Searches in PubMed, Scopus, Web of Science, and Embase databases were performed to recover studies, published until October 2022, with healthy children, which investigated the vitamin D status, related or not to undesirable bone alterations linked to bone quality (bone mineral density and bone mineral content), fracture or anthropometry. Country, study design, area of expertise (medicine, nutrition, dentistry, others), bone outcome, 25-hydroxyvitamin D data (serum or intake levels), the exams for bone diagnosis, and the results were analyzed in the VantagePoint^TM software. Results: Of 20,583 studies, 27 were included. The USA (n=9; 33.3%) had the highest number of publications. Cross-sectional (n=11; 40.7%), case-control (n=9; 33.3%), and cohort studies (n=7; 25.9%) contemplated the medicine and nutritional areas without any study in dentistry. Studies about bone quality (n=21; 77.8%), analyzed through dual-energy X-ray absorptiometry (DXA; n=14; 51.8%), with association (n=16; 59.2%) between the low serum levels of 25-hydroxyvitamin D and undesirable bone alterations (n=14; 51.8%) were the most prevalent. Conclusion: Most studies were conducted in the medical area and showed an association between low bone quality and low levels of 25-hydroxyvitamin D, verified through DXA.

References

Holick MF. Vitamin D deficiency. N Engl J Med 2007; 357(3):266-281. https://doi.org/10.1056/NEJMra070553

Holick MF. Vitamina D. São Paulo: Fundamento Educacional Ltda.; 2012. 352p. [In Portuguese].

Fisher L, Fisher A. Vitamin D and parathyroid hormone in outpatients with non-cholestatic chronic liver disease. Clin Gastroenterol Hepatol 2007; 5(4):513-520. https://doi.org/10.1016/j.cgh.2006.10.015

Premaor MO, Furlanetto TW. Hipovitaminose D em adultos: Entendendo melhor a apresentação de uma velha doença. Arq Bras Endocrinol Metabol 2006; 50(1):25-37. https://doi.org/10.1590/S0004-27302006000100005 [In Portuguese].

Rosen CJ, Abrams AS, Aloia JF, Brannon PM, Clinton SK, Durazo-Arvizu RA, et al. IOM committee members respond to Endocrine Society vitamin D guideline. J Clin Endocrinol Metab 2012; 97(4):1146-1152. https://doi.org/10.1210/jc.2011-2218

Shore RM, Chesney RW. Rickets: Part I. Pediatr Radiol 2013; 43(2):140-151. https://doi.org/10.1007/s00247-012- 2532-x

Hossein-Nezhad A, Holick MF. Vitamin D for health: A global perspective. Mayo Clin Proc 2013; 88(7):720-755. https://doi.org/10.1016/j.mayocp.2013.05.011

Elder CJ, Bishop NJ. Rickets. Lancet 2014; 383(9929):1665-1676. https://doi.org/10.1016/S0140-6736(13)61650-5

Winzenberg T, Jones G. Vitamin D and bone health in childhood and adolescence. Calcif Tissue Int 2013; 92(2):140- 150. https://doi.org/10.1007/s00223-012-9615-4

World Health Organization. Guidelines. Age Groups and Populations. Available from: https://apps.who.int/iris/rest/bitstreams/1336192/retrieve. [Accessed on March 17, 2023].

Al-Ghamdi MA, Lanham-New SA, Kahn JA. Differences in vitamin D status and calcium metabolism in Saudi Arabian boys and girls aged 6 to 18 years: effects of age, gender, extent of veiling and physical activity with concomitant implications for bone health. Public Health Nutr 2012;15(10):1845-53. https://doi.org/10.1017/S1368980011003612

Breen ME, Laing EM, Hall DB, Hausman DB, Taylor RG, Isales CM, et al. 25-hydroxyvitamin D, insulin-like growth factor-I, and bone mineral accrual during growth. J Clin Endocrinol Metab 2011; 96(1):E89-98. https://doi.org/10.1210/jc.2010-0595

Das S, Sanchez JJ, Alam A, Haque A, Mahfuz M, Ahmed T, et al. Dietary Magnesium, Vitamin D, and Animal Protein Intake and Their Association to the Linear Growth Trajectory of Children from Birth to 24 Months of Age: Results From MAL-ED Birth Cohort Study Conducted in Dhaka, Bangladesh. Food Nutr Bull 2020; 41(2):200-210. https://doi.org/10.1177/0379572119892408

El-Sakka A, Penon C, Hegazy A, Elbatrawy S, Gobashy A, Moreira A. Evaluating bone health in Egyptian children with forearm fractures: A case control study. Int J Pediatr 2016; 2016:7297092. https://doi.org/10.1155/2016/7297092

Filteau S, Rehman AM, Yousafzai A, Chugh R, Kaur M, Sachdev HP, et al. Associations of vitamin D status, bone health and anthropometry, with gross motor development and performance of school-aged Indian children who were born at term with low birth weight. BMJ Open 2016; 6(1):e009268. https://doi.org/10.1136/bmjopen-2015-009268

Fu Y, Hu Y, Qin Z, Zhao Y, Yang Z, Li Y, et al. Association of serum 25-hydroxyvitamin D status with bone mineral density in 0-7 year old children. Oncotarget 2016; 7(49):80811-80819. https://doi.org/10.18632/oncotarget.13097

Garcia AH, Erler NS, Jaddoe VWV, Tiemeier H, van den Hooven EH, Franco OH, et al. 25-hydroxyvitamin D concentrations during fetal life and bone health in children aged 6 years: a population-based prospective cohort study. Lancet Diabetes Endocrinol 2017; 5(5):367-376. https://doi.org/10.1016/S2213-8587(17)30064-5

Herrmann D, Pohlabeln H, Gianfagna F, Konstabel K, Lissner L, Mårild S, et al. Association between bone stiffness and nutritional biomarkers combined with weight-bearing exercise, physical activity, and sedentary time in preadolescent children. A case-control study. Bone. 2015; 78:142-9. https://doi.org/10.1016/j.bone.2015.04.043

James JR, Massey PA, Hollister AM, Greber EM. Prevalence of hypovitaminosis D among children with upper extremity fractures. J Pediatr Orthop 2013; 33(2):159-62. https://doi.org/10.1097/BPO.0b013e3182770bf7

Mäyränpää MK, Viljakainen HT, Toiviainen-Salo S, Kallio PE, Mäkitie O. Impaired bone health and asymptomatic vertebral compressions in fracture-prone children: a case-control study. J Bone Miner Res 2012; 27(6):1413-24. https://doi.org/10.1002/jbmr.1579

McVey MK, Geraghty AA, O'Brien EC, McKenna MJ, Kilbane MT, Crowley RK, et al. The impact of diet, body composition, and physical activity on child bone mineral density at five years of age-findings from the ROLO Kids Study. Eur J Pediatr 2020; 179(1):121-131. https://doi.org/10.1007/s00431-019-03465-x

Mercy J, Dillon B, Morris J, Emmerson AJ, Mughal MZ. Relationship of tibial speed of sound and lower limb length to nutrient intake in preterm infants. Arch Dis Child Fetal Neonatal Ed 2007; 92(5):F381-5. https://doi.org/10.1136/adc.2006.105742

Minkowitz B, Cerame B, Poletick E, Nguyen JT, Formoso ND, Luxenberg SL, et al. Morris-Essex Pediatric Bone Health Group. Low vitamin D lLevels are associated with need for surgical correction of pediatric fractures. J Pediatr Orthop 2017; 37(1):23-29. https://doi.org/10.1097/BPO.0000000000000587

Nguyen PM, Pham LV, Nguyen KT, Nguyen DP, Nguyen HD, Lai NV, et al. Vitamin D and bone mineral density status, and their correlation with bone turnover markers in healthy children aged 6-14 in Vietnam. Curr Pediatr Res 2020; 24(3):204-209.

Oladosu MA, Esan O, Oginni LM, Adegbehingbe OO, Adedeji TA. (2021). Predictive value of serum vitamin D3 level for forearm fractures among children in a tropical country: A case control study. J Clin Diag Res 2021; 15(1):RC01-RC04. https://doi.org/10.7860/JCDR/2021/44836.14453

Rajakumar K, Fernstrom JD, Janosky JE, Greenspan SL. Vitamin D insufficiency in preadolescent African American children. Clin Pediatr 2005; 44(8):683-692. https://doi.org/10.1177/000992280504400806

Ren J, Brann LS, Bruening KS, Scerpella TA, Dowthwaite JN. Relationships among diet, physical activity, and dual plane dual-energy X-ray absorptiometry bone outcomes in pre-pubertal girls. Arch Osteoporos 2017; 12(1):19. https://doi.org/10.1007/s11657-017-0312-9

Ryan LM, Teach SJ, Brandoli C, Singer SA, Wood R, Freishtat RJ, et al. Predictors of forearm fracture risk in African American children. J Investig Med 2011; 59(3):634-635.

Ryan LM, Chamberlain JM, Singer SA, Wood R, Tosi LL, Freishtat RJ, et al. Genetic influences on vitamin D status and forearm fracture risk in African American children. J Investig Med 2012a; 60(6):902-906. https://doi.org/10.2310/JIM.0b013e3182567e2a

Ryan LM, Teach SJ, Singer SA, Wood R, Freishtat R, Wright JL, et al. Bone mineral density and vitamin D status among African American children with forearm fractures. Pediatrics 2012b; 130(3):e553-560. https://doi.org/10.1542/peds.2012-0134

Ryan LM, Devaney JM, Gordish-Dressman H, Stevens MW, Tosi L. Clinical factors associated with vitamin d deficiency in African American children with forearm fractures. J Investig Med 2014; 62(4):769-769.

Sakamoto Y, Ishijima M, Nakano S, Suzuki M, Liu L, Tokita A, et al. Physiologic leg bowing is not a physiologic condition but instead is associated with vitamin D disorders in toddlers. Calcif Tissue Int 2020; 106(2):95-103. https://doi.org/10.1007/s00223-019-00619-9

Sayers A, Fraser WD, Lawlor DA, Tobias JH. 25-Hydroxyvitamin-D3 levels are positively related to subsequent cortical bone development in childhood: Findings from a large prospective cohort study. Osteoporos Int 2012; 23(8):2117-28. https://doi.org/10.1007/s00198-011-1813-9

Sharawat IK, Dawman L. Bone mineral density and its correlation with vitamin D status in healthy school-going children of Western India. Arch Osteoporos 2019;14(1):13. https://doi.org/10.1007/s11657-019-0568-3

Videhult FK, Öhlund I, Hernell O, West CE. Body mass but not vitamin D status is associated with bone mineral content and density in young school children in northern Sweden. Food Nutr Res 2016; 60:30045. https://doi.org/10.3402/fnr.v60.30045

White Z, White S, Dalvie T, Kruger MC, Van Zyl A, Becker P. Bone health, body composition, and vitamin D status of black preadolescent children in South Africa. Nutrients 2019; 11(6):1243. https://doi.org/10.3390/nu11061243

Yorifuji J, Yorifuji T, Tachibana K, Nagai S, Kawai M, Momoi T, et al. Craniotabes in normal newborns: the earliest sign of subclinical vitamin D deficiency. J Clin Endocrinol Metab 2008; 93(5):1784-8. https://doi.org/10.1210/jc.2007-2254

Thomas MK, Demay MB. Vitamin D deficiency and disorders of vitamin D metabolism. Endocrinol Metab Clin 2000; 29(3):611-627. https://doi.org/10.1016/s0889-8529(05)70153-5

Moore CE, Murphy MM, Holick MF. Vitamin D intakes by children and adults in the United States differ among ethnic groups. J Nutr 2005; 135(10):2478-2485. https://doi.org/10.1093/jn/135.10.2478

Wacker M, Holick MF. Sunlight and Vitamin D: A global perspective for health. Dermatoendocrinol 2013; 5(1):51- 108. https://doi.org/10.4161/derm.24494

Golden NH, Abrams SA. Committee on Nutrition Pediatrics. Optimizing bone health in children and adolescents. Pediatrics 2014; 134(4):e1229-1243. https://doi.org/10.1542/peds.2014-2173

Stagi S, Cavalli L, Iurato C, Seminara S, Brandi ML, de Martino M. Bone metabolism in children and adolescents: Main characteristics of the determinants of peak bone mass. Clin Cases Miner 2013; 10(3):172-179.

Miller PD, Zapalowski C, Kulak CAM, Bilezikian JP. Bone densitometry: The best way to detect osteoporosis and to monitor therapy. J Clin Endocr 1999; 84:1867-1871. https://doi.org/10.1210/jcem.84.6.5710

Baum T, Kutscher M, Muller D, Rath C, Eckstein F, Lochmuller EM, et al. Cortical and trabecular bone structure analysis at the distal radius-prediction of biomechanical strength by DXA and MRI. J Bone Miner Metab 2013; 31(2):212-221. https://doi.org/10.1007/s00774-012-0407-8

Waltzman ML, Shannon M, Bowen AP, Bailey MC. Monkeybar injuries: Complications of play. Pediatrics 1999; 103(5):e58. https://doi.org/10.1542/peds.103.5.e58

Stark AD, Bennet GC, Stone DH, Chishti P. Association between childhood fractures and poverty: Population-based study. BMJ 2002; 324(7335):457. https://doi.org/10.1136/bmj.324.7335.457

Galano GJ, Vitale MA, Kessler MK, Hyman JE, Vitale MG. The most frequent traumatic orthopaedic injuries from a national pediatric inpatient population. J Pediatr Orthop 2005; 25(1):39-44. https://doi.org/10.1097/00004694- 200501000-00010

Rodriguez-Merchan EC. Pediatric skeletal trauma: A review and historical perspective. Clin Orthop Relat Res 2005; 432:8-13.

Beaty JH, Rockwood CA, Kasser JR. Rockwood and Wilkins Fractures in Children. 7th ed. Philadelphia, PA: Wolters Kluwer/Lippincott, Williams & Wilkins; 2010, 292-444.

Goulding A, Grant AM, Williams SM. Bone and body composition of children and adolescents with repeated forearm fractures J Bone Miner Res 2005; 20(12):2090-2096. https://doi.org/10.1359/JBMR.050820

Goulding A, Cannan R, Williams SM, Gold EJ, Taylor RW, Lewis-Barned NJ. Bone mineral density in girls with forearm fractures. J Bone Miner Res 1998; 13(1):143-148. https://doi.org/10.1359/jbmr.1998.13.1.143

Goulding A, Jones IE, Taylor RW, Williams SM, Manning PJ. Bone mineral density and body composition in boys with distal forearm fractures: A dual-energy x-ray absorptiometry study. J Pediatr 2001; 139(4):509-515. https://doi.org/10.1067/mpd.2001.116297

Lehtonen-Veromaa MK, Möttönen TT, Nuotio IO, Irjala KM, Leino AE, Viikari JS. Vitamin D and attainment of peak bone mass among peripubertal Finnish girls: A 3-y prospective study. Am J Clin Nutr 2002; 76(6):1446-1453. https://doi.org/10.1093/ajcn/76.6.1446

Ma D, Jones G. The association between bone mineral density, metacarpal morphometry, and upper limb fractures in children: A population-based case-control study. J Clin Endocrinol 2003; 88(4):1486-1491. https://doi.org/10.1210/jc.2002-021682

Fischer PR, Thacher TD, Pettifor JM, Jorde LB, Eccleshall TR, Feldman D. Vitamin D receptor polymorphisms and nutritional rickets in Nigerian children. J Bone Miner Res 2000; 15(11):2206-2210. https://doi.org/10.1359/jbmr.2000.15.11.2206

NIH. Consensus development panel on osteoporosis prevention, diagnosis, and therapy. Osteoporosis prevention, diagnosis, and therapy. J Am Med Assoc 2001; 285(6):785-795. https://doi.org/10.1001/jama.285.6.785

Choi YJ. Dual-energy x-ray absorptiometry: Beyond bone mineral density determination. Endocrinol Metab 2016; 31(1):25-30. https://doi.org/10.3803/EnM.2016.31.1.25

ICRP. The 2007 Recommendations of the International Commission on Radiological Protection. ICRP publication 103. Annals of the ICRP 2007; 37(2-4):1-332. https://doi.org/10.1016/j.icrp.2007.10.003

Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Muller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 2010; 25(7):1468-1486. https://doi.org/10.1002/jbmr.141

Cheung AM, Adachi JD, Hanley DA, Kendler DL, Davison KS, Josse R, et al. High-resolution-peripheral quantitative computed tomography for the assessment of bone strength and structure: a review by the Canadian Bone Strength Working Group. Curr Osteoporos Rep 2013; 11(2):136-146. https://doi.org/10.1007/s11914-013-0140-9

Eckstein F, Matsuura M, Kuhn V, Priemel M, Müller R, Link TM, et al. Sex differences of human trabecular bone microstructure in aging are site-dependent. J Bone Miner Res 2007; 22(6):817-824. https://doi.org/10.1359/jbmr.070301

Barkmann R, Glüer CC. Quantitativer Ultraschall. Der Radiologe 2006; 46(10):861-869. https://doi.org/10.1007/s00117-006-1394-3

[63] Sichieri R, Everhart J. Validity of a Brazilian food frequency questionnaire against dietary recalls and estimated energy intake. Nutr Res 1998; 18(10):1649-1659. https://doi.org/10.1016/S0271-5317(98)00151-1

Cui Q, Xia Y, Wu Q, Chang Q, Niu K, Zhao Y. A meta-analysis of the reproducibility of food frequency questionnaires in nutritional epidemiological studies. Int J Behav Nutr Phys Act 2021; 18(1):12. https://doi.org/10.1186/s12966-020- 01078-4

Tsubono Y, Kobayashi M, Sasaki S, Tsugane S, JPHC. Validity and reproducibility of a self-administered food frequency questionnaire used in the baseline survey of the JPHC study cohort I. J Epidemiol 2003; 13(1 Suppl):S125-S133. https://doi.org/10.2188/jea.13.1sup_125

Männistö S, Virtanen M, Mikkonen T, Pietinen P. Reproducibility and validity of a food frequency questionnaire in a case-control study on breast cancer. J Clin Epidemiol 1996; 49(4):401-409. https://doi.org/10.1016/0895-4356(95)00551-X

Johnson L, Mander A, Jones L, Emmett P, Jebb S. A prospective analysis of dietary energy density at age 5 and 7 years and fatness at 9 years among UK children. Int J Obes 2008; 12(4):586-593. https://doi.org/10.1038/sj.ijo.0803746

Auld CRG, Heimendinger J, Hambidge C, Hambidge M. Outcomes from a school-based nutrition education program using resource teachers and cross-disciplinary models. J Nutr Educ 1998; 12(10):268-280. https://doi.org/10.1016/S0022-3182(98)70336-X

Eck L, Klesges R, Hanson C. Recall of a child’s intake from one meal: Are parents accurate? J Am Diet Assoc 1989; 12(6):784-789.

Cade J, Thompson R, Burley V, Warm D. Development, validation and utilisation of food-frequency questionnaires – A review. Public Health Nutr 2002; 5(4):567-587. https://doi.org/10.1079/phn2001318

Rezazadeh A, Omidvar N, Tucker KL. Food frequency questionnaires developed and validated in Iran: A systematic review. Epidemiol Health 2020; 42:e2020015. https://doi.org/10.4178/epih.e202001