We investigated bone mineral density (BMD) at different ages after the Fontan completion, and we evaluated the relationship between BMD, vitamin D levels, and pertinent patient variables.

Methods

A cross-sectional sample of 64 patients was examined with dual-energy X-ray absorptiometry (DXA) scans to determine BMD. Of these patients, 24 were also examined with BoneXpert software to determine bone mass density (BMX), expressed as the bone health index (BHI). Blood samples from all patients were analyzed. Patients were divided into three different age groups; A: 4-9 years old (n = 22), B: 10-15 years old (n = 21), and C: 16-18 years old (n = 21).

Results

Overall, BMD z scores were (mean ± SD): −1.0 ± 1.3 for the lumbar spine and −0.2 ± 1.2 for the total body. Groups B and C had significantly lower z score values compared to group A. Of patients in group C, 35% had z score values ≤−2 SD of the mean of the healthy population. There was no difference related to systemic ventricular anatomy (left or right); however, patients with lateral tunnels had lower BMD than patients with extra cardiac conduits. Overall, the BHI z score was (mean ± SD): −1.2 ± 0.9, but low BMX did not correlate with low BMD. The 25-hydroxy vitamin D level was 58 ± 30 nmol/L. Vitamin D levels decreased with age: in group C, 33.3% of patients exhibited vitamin D deficiencies. Vitamin D levels were not correlated with bone mineral densities.

Conclusion

BMD levels decreased with age in patients with Fontan circulation. Different bone components were involved. Vitamin D levels also decreased with age, but they were not consistently associated with bone mineral densities. The single factor most predictive of low BMD was a lateral tunnel Fontan, compared to an extra cardiac Fontan.

CONFLICTS OF INTEREST

The authors have no financial relationships relevant to this article to disclose. None of the authors have conflicts of interest to disclose.

References

1Mori M, Aguirre AJ, Elder RW, et al. Beyond a broken heart: circulatory dysfunction in the failing Fontan. Pediatr Cardiol. April 2014; 35(4): 569-579.
10.1007/s00246-014-0881-y
PubMed Web of Science® Google Scholar
2Rychik J, Goldberg DJ. Late consequences of the Fontan operation. Circulation. October 21 2014; 130(17): 1525-1528.
10.1161/CIRCULATIONAHA.114.005341
PubMed Web of Science® Google Scholar
3Book WM, Gerardin J, Saraf A, Marie Valente A, Rodriguez F 3rd. Clinical phenotypes of Fontan failure: implications for management. Congenit Heart Dis. July 2016; 11(4): 296-308.
10.1111/chd.12368
PubMed Web of Science® Google Scholar
4Rychik J, Atz AM, Celermajer DS, et al. Evaluation and management of the child and adult with Fontan circulation: a scientific statement from the American Heart Association. Circulation. July 1 2019; 140:CIR0000000000000696.
10.1161/CIR.0000000000000696
Web of Science® Google Scholar
5D'Ambrosio P, Tran D, Verrall CE, et al. Prevalence and risk factors for low bone density in adults with a Fontan circulation. Congenit Heart Dis. August 20 2019, 1-9. https://doi.org/10.1111/chd.12836.
Web of Science® Google Scholar
6McCrindle BW, Williams RV, Mital S, et al. Physical activity levels in children and adolescents are reduced after the Fontan procedure, independent of exercise capacity, and are associated with lower perceived general health. Arch Dis Child. June 2007; 92(6): 509-514.
10.1136/adc.2006.105239
PubMed Web of Science® Google Scholar
7Leonard MB. Glucocorticoid-induced osteoporosis in children: impact of the underlying disease. Pediatrics. March 2007; 119(Suppl 2): S166-S174.
10.1542/peds.2006-2023J
PubMed Web of Science® Google Scholar
8Bishop N, Arundel P, Clark E, et al. Fracture prediction and the definition of osteoporosis in children and adolescents: the ISCD 2013 Pediatric Official Positions. J Clin Densitom. April–June 2014; 17(2): 275-280.
10.1016/j.jocd.2014.01.004
PubMed Web of Science® Google Scholar
9Godang K, Qvigstad E, Voldner N, et al. Assessing body composition in healthy newborn infants: reliability of dual-energy x-ray absorptiometry. J Clin Densitom. April–June 2010; 13(2): 151-160.
10.1016/j.jocd.2010.01.121
PubMed Web of Science® Google Scholar
10Crabtree NJ, Arabi A, Bachrach LK, et al. Dual-energy X-ray absorptiometry interpretation and reporting in children and adolescents: the revised 2013 ISCD Pediatric Official Positions. J Clin Densitom. April–June 2014; 17(2): 225-242.
10.1016/j.jocd.2014.01.003
PubMed Web of Science® Google Scholar
11van Rijn RR, Lequin MH, Thodberg HH. Automatic determination of Greulich and Pyle bone age in healthy Dutch children. Pediatr Radiol. June 2009; 39(6): 591-597.
10.1007/s00247-008-1090-8
PubMed Web of Science® Google Scholar
12Thodberg HH. Clinical review: an automated method for determination of bone age. J Clin Endocrinol Metab. July 2009; 94(7): 2239-2244.
10.1210/jc.2008-2474
CAS PubMed Web of Science® Google Scholar
13Thodberg HH, Savendahl L. Validation and reference values of automated bone age determination for four ethnicities. Acad Radiol. November 2010; 17(11): 1425-1432.
10.1016/j.acra.2010.06.007
PubMed Web of Science® Google Scholar
14Thodberg HH, van Rijn RR, Tanaka T, Martin DD, Kreiborg S. A paediatric bone index derived by automated radiogrammetry. Osteoporos Int. August 2010; 21(8): 1391-1400.
10.1007/s00198-009-1085-9
CAS PubMed Web of Science® Google Scholar
15Anink J, Nusman CM, van Suijlekom-Smit LW, van Rijn RR, Maas M, van Rossum MA. Automated determination of bone age and bone mineral density in patients with juvenile idiopathic arthritis: a feasibility study. Arthritis Res Ther. August 2014; 16(4): 424.
10.1186/s13075-014-0424-1
PubMed Web of Science® Google Scholar
16Munns CF, Shaw N, Kiely M, et al. Global consensus recommendations on prevention and management of nutritional rickets. J Clin Endocrinol Metab. February 2016; 101(2): 394-415.
10.1210/jc.2015-2175
CAS PubMed Web of Science® Google Scholar
17Płudowski P, Lebiedowski M, Lorenc RS. Evaluation of practical use of bone age assessments based on DXA-derived hand scans in diagnosis of skeletal status in healthy and diseased children. J Clin Densitometry. 2005; 8(1): 48-56.
10.1385/JCD:8:1:048
PubMed Web of Science® Google Scholar
18Creo AL, Schwenk WF. Age: a handy tool for pediatric providers. Pediatrics. December 2017; 140(6):e20171486.
10.1542/peds.2017-1486
PubMed Web of Science® Google Scholar
19Levine MA. Assessing bone health in children and adolescents. Indian J Endocrinol Metab. December 2012; 16(Suppl 2): S205-S212.
PubMed Google Scholar
20Joseph S, McCarrison S, Wong SC. Skeletal fragility in children with chronic disease. Horm Res Paediatr. 2016; 86(2): 71-82.
10.1159/000447583
CAS PubMed Web of Science® Google Scholar
21Holick MF. Vitamin D deficiency. N Engl J Med. July 2007; 357(3): 266-281.
10.1056/NEJMra070553
CAS PubMed Web of Science® Google Scholar
22Misra M, Pacaud D, Petryk A, et al. Vitamin D deficiency in children and its management: review of current knowledge and recommendations. Pediatrics. August 2008; 122(2): 398-417.
10.1542/peds.2007-1894
PubMed Web of Science® Google Scholar
23Saraff V, Hogler W. Endocrinology and adolescence: osteoporosis in children: diagnosis and management. Eur J Endocrinol. December 2015; 173(6): R185-R197.
10.1530/EJE-14-0865
CAS PubMed Web of Science® Google Scholar
24Lu J, Shin Y, Yen MS, Sun SS. Peak bone mass and patterns of change in total bone mineral density and bone mineral contents from childhood into young adulthood. J Clin Densitom. April–June 2016; 19(2): 180-191.
10.1016/j.jocd.2014.08.001
PubMed Web of Science® Google Scholar
25Wildman S, Henwood-Finlay M. Pediatric DXA: a review of proper technique and correct interpretation. J Am Osteopath Coll Radiol. 2012; 3: 17-26.
Google Scholar
26Goldberg DJ, Dodds K, Avitabile CM, et al. Children with protein-losing enteropathy after the Fontan operation are at risk for abnormal bone mineral density. Pediatr Cardiol. December 2012; 33(8): 1264-1268.
10.1007/s00246-012-0290-z
PubMed Web of Science® Google Scholar
27Avitabile CM, Goldberg DJ, Zemel BS, et al. Deficits in bone density and structure in children and young adults following Fontan palliation. Bone. August 2015; 77: 12-16.
10.1016/j.bone.2015.04.012
PubMed Web of Science® Google Scholar
28Nusman CM, Anink J, Otten MH, et al. Bone health of patients with juvenile idiopathic arthritis: a comparison between dual-energy X-ray absorptiometry and digital X-ray radiogrammetry. Eur J Radiol. October 2015; 84(10): 1999-2003.
10.1016/j.ejrad.2015.06.015
PubMed Web of Science® Google Scholar
29Alshamrani K, Messina F, Bishop N, Offiah AC. Estimating bone mass in children: can bone health index replace dual energy x-ray absorptiometry? Pediatr Radiol. March 2019; 49(3): 372-378.
10.1007/s00247-018-4309-3
PubMed Web of Science® Google Scholar
30Dubner SE, Shults J, Baldassano RN, et al. Longitudinal assessment of bone density and structure in an incident cohort of children with Crohn's disease. Gastroenterology. January 2009; 136(1): 123-130.
10.1053/j.gastro.2008.09.072
PubMed Web of Science® Google Scholar
31Lin Z, Ge H, Xue J, et al. Comparison of extracardiac conduit and lateral tunnel for functional single-ventricle patients: a meta-analysis. Congenit Heart Dis. December 2017; 12(6): 711-720.
10.1111/chd.12503
PubMed Web of Science® Google Scholar
32Ben Ali W, Bouhout I, Khairy P, Bouchard D, Poirier N. Extracardiac versus lateral tunnel Fontan: a meta-analysis of long-term results. Ann Thorac Surg. March 2019; 107(3): 837-843.
10.1016/j.athoracsur.2018.08.041
PubMed Web of Science® Google Scholar
33Bocsi J, Lenz D, Sauer U, et al. Inflammation and immune suppression following protein losing enteropathy after Fontan surgery detected by cytomics. Trans Med Hemotherapy. 2007; 34(3): 168-175.
10.1159/000101396
Web of Science® Google Scholar
34Avitabile CM, Leonard MB, Brodsky JL, et al. Usefulness of insulin like growth factor 1 as a marker of heart failure in children and young adults after the Fontan palliation procedure. Am J Cardiol. March 15 2015; 115(6): 816-820.
10.1016/j.amjcard.2014.12.041
CAS PubMed Web of Science® Google Scholar
35Hedstrom EM, Svensson O, Bergstrom U, Michno P. Epidemiology of fractures in children and adolescents. Acta Orthop. February 2010; 81(1): 148-153.
10.3109/17453671003628780
PubMed Web of Science® Google Scholar
36Anderson PAW, Sleeper LA, Mahony L, et al. Contemporary outcomes after the Fontan procedure: a Pediatric Heart Network multicenter study. J Am Coll Cardiol. July 8 2008; 52(2): 85-98.
10.1016/j.jacc.2008.01.074
PubMed Web of Science® Google Scholar
37Płudowski P, Karczmarewicz E, Bayer M, et al. Practical guidelines for the supplementation of vitamin D and the treatment of deficits in Central Europe — recommended vitamin D intakes in the general population and groups at risk of vitamin D deficiency. Endokrynologia Polska. 2013; 64(4): 319-327.
10.5603/EP.2013.0012
CAS PubMed Web of Science® Google Scholar
38Holler F, Hannes T, Germund I, et al. Low serum 25-hydroxyvitamin D levels and secondary hyperparathyroidism in Fontan patients. Cardiol Young. June 2016; 26(5): 876-884.
10.1017/S1047951115001444
PubMed Web of Science® Google Scholar
39Absoud M, Cummins C, Lim MJ, Wassmer E, Shaw N. Prevalence and predictors of vitamin D insufficiency in children: a Great Britain population based study. PLoS ONE. 2011; 6(7):e22179.
10.1371/journal.pone.0022179
CAS PubMed Web of Science® Google Scholar
40Moon RJ, Harvey NC, Davies JH, Cooper C. Vitamin D and skeletal health in infancy and childhood. Osteoporos Int. December 2014; 25(12): 2673-2684.
10.1007/s00198-014-2783-5
CAS PubMed Web of Science® Google Scholar
41Mayranpaa MK, Viljakainen HT, Toiviainen-Salo S, Kallio PE, Makitie O. Impaired bone health and asymptomatic vertebral compressions in fracture-prone children: a case-control study. J Bone Miner Res. June 2012; 27(6): 1413-1424.
10.1002/jbmr.1579
PubMed Web of Science® Google Scholar
42Ceroni D, Anderson de la Llana R, Martin X, et al. Prevalence of vitamin D insufficiency in Swiss teenagers with appendicular fractures: a prospective study of 100 cases. J Child Orthop. 2012; 6(6): 497-503.
10.1007/s11832-012-0446-7
PubMed Google Scholar

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Progressive loss of bone mass in children with Fontan circulation

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Progressive loss of bone mass in children with Fontan circulation

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Objective

Methods

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