Unaffected bone mineral density in Danish children and adolescents with type 1 diabetes
Adults with type 1 diabetes mellitus (T1D) have decreased bone mineral density (BMD). Our study aimed at determining BMD and the association to metabolic control in children and adolescents with T1D.
244 patients (113 girls) with a median age of 14.3 years and T1D duration of 1–16 years were included. A dual-energy X-ray absorptiometry scan assessed BMD Z-scores excluding the head (total body less head, TBLH). TBLH-BMD were then investigated for associations to diabetes relevant variables such as HbA1c, insulin treatment, anthropometry and physical activity.
In all participants the TBLH-BMD Z-score (0.22 ± 0.96) was significantly higher than the references. Separated by sex, TBLH-BMD Z-score in boys (0.11 ± 0.84) was no different from healthy peers whereas TBLH-BMD Z-score was significantly higher in girls (0.36 ± 1.09). The higher TBLH-BMD Z-score in girls were explained by higher BMI Z-scores. Participants with assumed final height (based on age) had an average TBLH-BMD Z-score of 0.78 ± 1.06, significantly higher than references independent of gender, HbA1c, height- and weight Z-scores. Multiple regression analyses showed that TBLH BMD Z-score associated negatively to HbA1c (P = 0.003), pump treatment (P = 0.019) and screen-time (P = 0.005) and positively to weight Z-score (P < 0.001). Physical activity, sex and puberty did not significantly associate to TBLH-BMD Z-score.
Unlike adults with T1D, BMD is not decreased in children and adolescents with T1D and even elevated after attained final height. As HbA1c negatively associates to BMD, decreased BMD may progress over time. Whether changes in microarchitecture or bone metabolism precede changes in BMD needs further investigation.
KeywordsBone mineral density Pediatrics Type 1 diabetes mellitus HbA1c
Type 1 diabetes mellitus
Bone mineral density
Bone mineral content
Glycated haemoglobin A1c
Type 2 diabetes mellitus
Dual energy X-ray absorptiometry
Peripheral quantitative computed tomography
Total body less head bone mineral density
Fasting blood glucose
International Society of Clinical Densitometry
Akaike information criterion
Continuous subcutaneus insulin infusion
Multiple daily injections
Body mass index
Jette Høgsmose and Sussi Polmann for lending their expertise in blood sample acquisition and handling.
JOBM and JJ have designed the study and been the main writers of the article. AKJ have contributed with statistical help and understanding to optimize the statistics section. BZ and NRJ have contributed with expertise on bone health and bone examination in general. BSO and FP have been important parts of study development and design and finally CWH have gathered all data together with JOBM. All authors have contributed with proof-reading and constructive comments in putting together this manuscript.
This work was supported by Aase og Ejnar Danielssens fond (10-001544), Dronning Louises Børnehospitals fond, Vissing Fonden, Poul og Erna Sehested Hansens Fond (DK), Sehested Hansen Fonden and The research council at Herlev and Gentofte Hospital.
Compliance with ethical standards
Conflict of interest
All authors have no conflicts of interest.
- 3.Léger J, Marinovic D, Alberti C, Dorgeret S, Chevenne D, Marchal CL, Tubiana-Rufi N, Sebag G, Czernichow P (2006) Lower bone mineral content in children with type 1 diabetes mellitus is linked to female sex, low insulin-like growth factor type I levels, and high insulin requirement. J Clin Endocrinol Metab 91:3947–3953PubMedCrossRefGoogle Scholar
- 8.Khoshhal KI, Sheweita SA, Al-Maghamsi MS, Habeb AM (2015) Does type 1 diabetes mellitus affect bone quality in prepubertal children? J Taibah Univ Med Sci 10:300–305Google Scholar
- 19.Vargas DM, Rigotti T, Gütz CNRM, Lobe MCS, de Fernades JA (2003) Bone mineralization in children and adolescents with type 1 diabetes. J Pediatr (Rio J) 79:253–258Google Scholar
- 22.Abo-El-Asrar M, Farid S, El Maraghy M, Mohamedeen A (2011) Serum osteocalcin, zinc nutritive status and bone turnover in children and adolescents with type 1 diabetes mellitus. J Diabetes Metab 2:128Google Scholar
- 32.Crabtree NJ, Arabi A, Bachrach LK, Fewtrell M, El-Hajj Fuleihan G, Kecskemethy HH, Jaworski M, Gordon CM (2014) Dual-energy X-ray absorptiometry interpretation and reporting in children and adolescents: the revised 2013 ISCD Pediatric Official Positions. J Clin Densitom Off J Int Soc Clin Densitom 17:225–242CrossRefGoogle Scholar
- 37.Tinggaard J, Aksglaede L, Sørensen K, Mouritsen A, Wohlfahrt-Veje C, Hagen CP, Mieritz MG, Jørgensen N, Wolthers OD, Heuck C, Pedersen JH, Main KM, Juul A (2014) The 2014 Danish references from birth to 20 years for height, weight and body mass index. Acta Paediatr 103:214–224PubMedCrossRefGoogle Scholar
- 38.Svensson J, Schwandt A, Pacaud D, Beltrand J, Birkebaek NH, Cardona-Hernandez R, Casteels K, Castro S, Cherubini V, Cody D, Fisch N, Hasnani D, Kordonouri O, Kosteria I, Luczay A, Pundziute-Lyckå A, Maffeis C, Piccini B, Luxmi P, Sumnik Z, de Beaufort C (2018) The influence of treatment, age at onset, and metabolic control on height in children and adolescents with type 1 diabetes—a SWEET collaborative study. Pediatr Diabetes 19:1441–1450PubMedCrossRefGoogle Scholar
- 41.Shanbhogue VV, Hansen S, Frost M, Jørgensen NR, Hermann AP, Henriksen JE, Brixen K (2015) Bone geometry, volumetric density, microarchitecture, and estimated bone strength assessed by HR-pQCT in adult patients with type 1 diabetes mellitus. J Bone Miner Res Off J Am Soc Bone Miner Res 30:2188–2199CrossRefGoogle Scholar