Effect of body composition on bone mineral density in Moroccan patients with juvenile idiopathic arthritis
Dalal El Badri, Samira Rostom, Ilham Bouaddi, Asmae Hassani, Bouchra Chkirate, Bouchra Amine, Najia Hajjaj-Hassouni
Corresponding author: Dalal El Badri, Department of Rheumatology , EL Ayachi Hospital, University Hospital of Rabat-Sale, 11000, Sale, Morocco
Received: 25 Jun 2012 - Accepted: 31 Aug 2012 - Published: 18 Feb 2014
Domain: Clinical medicine
Keywords: Body composition, lean mass, fat mass, juvenile idiopathic arthritis
©Dalal El Badri et al. Pan African Medical Journal (ISSN: 1937-8688). This is an Open Access article distributed under the terms of the Creative Commons Attribution International 4.0 License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Cite this article: Dalal El Badri et al. Effect of body composition on bone mineral density in Moroccan patients with juvenile idiopathic arthritis. Pan African Medical Journal. 2014;17:115. [doi: 10.11604/pamj.2014.17.115.1838]
Available online at: https://www.panafrican-med-journal.com//content/article/17/115/full
Original article
Effect of body composition on bone mineral density in Moroccan patients with juvenile idiopathic arthritis
Effect of body composition on bone mineral density in Moroccan patients with juvenile idiopathic arthritis
Dalal El Badri1,&, Samira Rostom1, Ilham Bouaddi1, Asmae Hassani1, Bouchra Chkirate2, Bouchra Amine1, Najia Hajjaj-Hassouni1
1Department of Rheumatology , EL Ayachi Hospital, University Hospital of Rabat-Sale, 11000, Sale, Morocco, 2Department of Pediatrics, children’s Hospital, University Hospital of Rabat-Sale, 11000, Rabat, Morocco
&Corresponding author
Dalal EL Badri, Department of Rheumatology , EL Ayachi Hospital, University Hospital of Rabat-Sale, 11000, Sale, Morocco
Introduction: The link between bone mass and body composition is widely recognized, but only few works were selectively performed on subjects with juvenile idiopathic arthritis. The aim of our study was to investigate the effect of body composition on bone mineral density (BMD) in Moroccan patients with juvenile idiopathic arthritis.
Methods: Thirty three children with juvenile idiopathic arthritis (JIA) were included in a cross-sectional study. The diagnosis of JIA was made according to the criteria of the International League of Association of Rheumatology (ILAR). Body mass index (BMI) was calculated from the ratio of weight/height2 (kg/m2). Pubertal status was determined according to the Tanner criteria. Bone status, body composition and bone mineral content (BMC) were analyzed by using dual-energy X-ray absorptiometry (DXA). BMD was assessed at the lumbar spine (L1-L4) and at total body in (g/cm2). Total body fat tissue mass (FTM) and lean tissue mass (LTM) were also analyzed by DXA and expressed in kilograms. In children, low BMD was defined as a Z-score less than -2 and osteoporosis was defined as a Z-score less than -2 with a fracture history.
Results: A cross-sectional study was conducted in 33 Moroccan patients with JIA aged between 4 and 16 years, Fat mass was not related to bone density; in contrast, BMD was positively associated to LTM in total body(r==0.41, p= 0.04) but not in lumbar spine (r=0.29, p= 0.17). There exist significant correlation between BMC and BMD in total body (r=0.51, p=0.01).
Conclusion: This study suggests that the LTM is a determining factor of the BMD during adolescence. Other studies with a broader sample would be useful to confirm this relation.
Childhood and adolescence are crucial periods for maximum bone mass acquisition, which is associated with genetic potential, nutritional factors, physical activity, and body composition [1]. Juvenile idiopathic arthritis (JIA) is comprised of a heterogeneous group of several disease subtypes that are characterized by the onset of arthritis prior to the age of 16 years; it's one of the commonest rheumatic diseases of children and an important cause of short- and long-term disability [2-5]. Osteoporosis is commonly observed in children with JIA [6] who are prone to changes in body composition because of disease and treatment related factors [7]. Deficits of muscle mass have been described as a central factor in (secondary) bone loss [8,9]. Apart from low bone mineral density (BMD) and lean mass, a higher fat mass was reported in children with rheumatic diseases [10]. In adults, this is summarized as rheumatoid cachexia [11]. Last years researches brought evidence for a strong relationship between body composition and bone mass [12]. However, association studies between body composition and BMD gave conflicting results, some reports showing a positive correlation between fat mass (FM) and BMD [13,14], while no association [15] was obtained by others, only few works were selectively performed on subjects with JIA. The aim of our study was to evaluate the influence of body composition parameters on peak bone mass in a group of Moroccan children with JIA.
Patients
This cross- sectional study was conducted in 33 children and adolescents, aged between 6 and 16 years, with JIA, currently observed at the Children's Hospital and department of Rheumatology of the University Hospital of Rabat-Sale Morocco. The diagnosis of JIA was made according to the criteria of International League of Associations for Rheumatology (ILAR) [16]. Parental consent was obtained from all participants. None of the subjects in this study had a medical history of chronic disease (endocrinal, neurological, cardiac, and renal) and no patient was taking bone sparing drugs.
The medical records of these patients were reviewed and information on the following parameters was extracted: age, sex, personal or family antecedent of fracture, subtype of JIA, disease duration, corticosteroid requirement (duration of corticosteroid use, cumulative corticosteroid dose calculated in mg as the product of mean daily dose × 365 × duration in years), requirement for and duration of other medications : methotrexate, salazopyrine and non-steroidal anti-inflammatory drugs (NSAIDs), Calcium and vitamin D supplementation. The functional disability was assessed by the Moroccan version of Childhood Health Assessment Questionnaire (CHAQ) [17], and the disease activity by the tender and swollen joint counts, patient assessment of pain and global disease activity, physician assessment of global disease activity, erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), disease activity score (DAS 28) for polyarticular and oligoarticular JIA [18], the Maastricht AS Enthesitis Score and Bath AS Disease Activity Index (BASDAI) for juvenile spondylarthropathy [19].
Pubertal status (pre- or postpubertal) was determined using breast and pubic hair stages in girls, testicular and pubic hair stages in boys, according to the Tanner criteria [20]. The participant's weight was measured in kg using a digital scale. Height was measured in meters using a vertical stadiometer. Based on these data, BMI (kg/m2) was calculated and it was also expressed as BMI-Z score, according to the World Health Organization Child Growth Standards (WHO) [21].
BMD measurement
Bone mineral density (BMD), bone mineral content (DMC) and body composition were analyzed by a single physician using the same dual energy radiography absorptiometry (DEXA), using (Lunar Prodigy; GE Lunar, Madison, WI) equipped with standard density software. Total body fat mass and lean mass were analyzed by DXA and expressed in kilograms. Bone mineral density of the L1-L4 lumbar spine and total body was evaluated in grams/centimeter2 and expressed as Z score for age, sex and ethnicity according to the reference data given for this equipment.
According to the International Society for Clinical Densitometry recommendations osteoporosis was defined as a Z-score less than -2 with a fracture history. Low BMD was defined as a Z-score less than -2 without a significant fracture history and osteoporosis was defined as a Z-score less than -2 with a fracture history [22-23]. Medical history for bone fractures was negative in all patients. All subjects underwent plain Vertebral Fracture Assessment (VFA) [24] to exclude unknown vertebral fractures.
Statistical analysis
Statistical analysis was performed using a software program (SPSS for Windows, Version 13.0, SPSS Inc, Chicago, IL). The data were expressed as the mean ± SD for continuous variables and as frequency (%) for categorical variables. Pearson or Spearman correlation coefficients were calculated to express association of continuous data with parametric or non-parametric distribution. One-way Anova was used to calculate differences between means. P values <0.05 were considered statistically significant.
Demographic and disease characteristics
The study included 33 patients (15 females) with a median age of 11(5.75-14)years and median disease duration of 2(1-4.5) years. Twelve of the patients were at prepubertal and thirteen were at pubertal period. The medians for weight, height, and BMI were -1 (-2.05-0) SD and -1(-2.5-0) SD, 5(2-6) SD respectively. Obesity (BMI> +2.0) was detected in 5 (15.15%) of the patients, 22.2% (4/18) of the boys and 6.66%% (1/15) of the girls. The socio-demographic and clinical characteristics of the patients are presented in Table 1.
Bone mineral density
Eleven patients (33.3%) were given a diagnosis of low BMD in lumbar spine, and nine (27%) in total body (Z-score < -2), and no patient was given a diagnosis of osteoporosis (Z-score < -2 and a significant fracture history) (Figure 1). The median of lean tissue mass (LTM), total body fat tissue mass (FTM) and bone mineral content (BMC) were 19001g (13827-33140)4930 g (3385- 9139)and 1044.90 g (630.40-1808.90) respectively. The mean Z-score of obesity group was 0.08±0.93. The BMD and Z scores of patients according to BMI are presented in Table 2.
Variables associated with parameters of body composition
LTM was correlated with age and Tanner stage. However we didn't find any correlation between these parameters and FTM (Table 3). Bone mineral density in total body was positively associated to LM in our study (r=0.41; p=0.04). In contrast, FM was not related to BMD of the lumbar spine and total body (Table 3).
In this analysis of the relationship between body composition parameters and BMD in Moroccan patients with JIA, a positive association was observed between LM, BMC and BMD, and no correlation was found between FM and BMD consistent with previous studies suggesting that LM represents an important determinant of cortical bone mass accrual in childhood [25-27]. In a study on the relationship between lean and fat mass and bone mineral in young adults and adolescents, Janicka et al. found that lean mass, but not FM was associated with BMD, suggesting that muscle mass is the major body composition parameter stimulating bone mineral acquisition [28].
Previous studies indicated that regardless of age or gender, lean mass has a strong positive influence on BMD [29]. However, the results of previous studies on the relation between fat mass and BMD were conflicting. Adipose tissue can be a weaker positive predictor [29] or stronger predictor [30] than lean mass, or even a negative predictor of BMD [28].
Low fracture risk in obese people suggests a role of fat tissue in maintaining bone mass, either mediated by mechanical loading or due to bone-active adipokines such as leptin [12]. Leptin has been proposed to be a mediator of adipose tissue hormonal effect on bone mass [31]. The role of leptin in bone metabolism is not fully understood, but in animal studies, leptin deficient mice have demonstrated a high bone mass phenotype [32].
Studies on body composition in inflammatory disease are more frequent in RA. In general, these studies have shown greater lean mass loss, especially in those with higher activity of disease and disability [33]. In adult patients with rheumatic arthritis, the abnormalities of body composition have been termed as rheumatoid cachexia [34].
Tumor necrosis factor-α seems to be a central mediator of muscle wasting [35]. Low physical activity predisposes the body to fat gain and is believed to precipitate a negative reinforcing cycle of loss of muscle mass [36].
In children with JIA, especially in severe forms, smaller increases in lean mass, larger gain in fat mass and lower bone mineral content were found, compared with healthy controls [37-39].
In our study, we find that BMC increased with age, puberty stage, and BMI, De Schepper et al. in a study conducted in136 normal growing children between the ages of 1 and 18 yr found that BMC increased more rapidly during puberty. For the entire group, the increase in BMC with age, height, and weight was best predicted by an exponential regression line analysis [40].
To our knowledge, the present study is the first to report effect of body composition on bone mineral density in Moroccan children with JIA but it should be noted that the cross sectional nature of this study limits the interpretation of our results especially to infer causality. Another limitation is the luck of a group of healthy participants.
In conclusion, in Moroccan patients with JIA, lean mass has a favorable effect on BMD. Fat mass seems not to protect the bone structure against osteoporosis. Further prospective studies with healthy participants are necessary to confirm our findings.
The authors declared no competing interests.
All authors contributed to the manuscript in conformity with ICMJE authorship criteria. All the authors have read and approved the final version of the manuscript.
Table 1: Socio-demographic and clinical characteristics of the patients
Table 2:
Bone mineral density and Z scores of patients according to BMI
Table 3: Correlation between body composition and clinical characteristics of patients
Table 4:
Relationships between body composition parameters and bone mineral density
Figure 1: Bone
mineral density on the patients with juvenile idiopathic arthritis in lumbar
spine and total
body
- Bouillon R, Prodonova A. Growth and hormone deficiency and peak bone mass. J Pediatr Endocrinol Metab. 2000; 13(6):1327-1336. PubMed | Google Scholar
- Cassidy JT, Petty RE. Chronic arthritis in childhood in: Textbook of Pediatric Rheumatology, 5th ed. Cassidy JT, Petty RE (eds). 2005. Philadelphia. Elsevier Saunders.
- Singh S. Chronic arthritis: current perspectives (editorial). Indian Pediatr. 2003; 40(5): 393-7. PubMed | Google Scholar
- Ravelli A, Martini A. Juvenile idiopathic arthritis. Lancet. 2007; 369(9563): 767-78. PubMed | Google Scholar
- Singh S. Collagen vascular disorders, in: Essential Pediatrics, 6th ed. Ghai OP, Gupta P, Paul VK (eds). 2004. New Delhi. CBS Publishers.
- Bardare M, Bianchi ML, Furia M, Gandolini GG, et al. Bone mineral metabolism in juvenile chronic arthritis: the influence of steroids. Clin Exp Rheumatol. 1991; 9(6):29-31. PubMed | Google Scholar
- K Markula-Patjas, O Mäkitie. Increased body adiposity in severe juvenile idiopathic arthritis. Bone. 2011; 48(2): S263. PubMed | Google Scholar
- Bechtold S, Ripperger P, Dalla Pozza R, Schmidt H, et al. Musculoskeletal and functional muscle-bone analysis in children with rheumatic disease using peripheral quantitative computed tomography. Osteoporos Int. 2005; 16(7):757-763. PubMed | Google Scholar
- Roth J, Palm C, Scheunemann I, Ranke MB, et al. Musculoskeletal abnormalities of the forearm in patients with juvenile idiopathic arthritis relate mainly to bone geometry. Arthritis Rheum. 2004; 50(4):1277-1285. PubMed | Google Scholar
- Mul D, van Suijlekom-Smit LW, ten Cate R, Bekkering WP, et al. Bone mineral density and body composition and influencing factors in children with rheumatic diseases treated with corticosteroids. J Pediatr Endocrinol Metab. 2002; 15(2):187-192. PubMed | Google Scholar
- Rall LC, Roubenoff R. Rheumatoid cachexia: metabolic abnormalities, mechanisms and interventions. Rheumatology (Oxford). 2004 Oct;43(10):1219-23. PubMed | Google Scholar
- Carmen Emanuela Georgescu, Ioana Ilie, Ileana Duncea. Association between body composition and bone mineral density in healthy, non-obese, young Romanian adults and effects of menopause. Maedica (Buchar). 2010; 5(1): 24-27. PubMed | Google Scholar
- St-Pierre DH, Faraj M, Karelis AD, et al. Lifestyle behaviours and components of energy balance as independent predictors of ghrelin and adiponectin in young non-obese women. Diabetes Metab. 2006;32(2):131-139. PubMed | Google Scholar
- Kanis JA, Johnell O, Oden A, et al. FRAX and the assessment of fracture probability in men and women from the UK. Osteoporos Int. 2008;19(4):385-397. PubMed | Google Scholar
- MacInnis RJ, Cassar C, Nowson CA, et al. Determinants of bone density in 30- to 65-year-old women: a co-twin study. J Bone Miner Res. 2003;18(9):1650-1656. PubMed | Google Scholar
- International League of Associations for Rheumatology. Classification of juvenile idiopathic arthritis: second revision, Edmonton, 2001. J Rheumatol. 2004; 31(2):390-2. PubMed | Google Scholar
- Rostom S, Amine B, Bensabbah R, Chkirat B, Abouqal R, Hajjaj-Hassouni N. Psychometric properties evaluation of the childhood health assessment questionnaire (CHAQ) in Moroccan juvenile idiopathic arthritis. Rheumatol Int. 2010; 30 (7):879-85. PubMed | Google Scholar
- Ringold S, Yun Chon, and Nora G. Singer. Associations between the American College of Rheumatology Pediatric Response Measures and the Continuous Measures of Disease Activity Used in Adult Rheumatoid Arthritis. Arthritis & Rheumatism. 2009; 60(12): 3776-3783. PubMed | Google Scholar
- Viswanath V, Myles A, Dayal R, Aggarwal A. Levels of Serum Matrix Metalloproteinase-3 Correlate with Disease Activity in the Enthesitis-related Arthritis Category of Juvenile Idiopathic Arthritis. J Rheumatol. 2011; 38 (11):2482-7. PubMed | Google Scholar
- Tanner JM. Physical growth and development. 1978. Churchill Livingstone. Edinburgh, Scotland. PubMed | Google Scholar
- WHO. The WHO Child Growth Standards. 2012. http://www.who.int/childgrowth/standards/en/. Accessed 22 February 2012.
- Lewiecki EM, Gordon CM, Baim S, Leonard MB, Bishop NJ, Bianchi ML, et al. International Society for Clinical Densitometry 2007 adult and pediatric official positions. Bone. 2008; 43(6): 1115-21. PubMed | Google Scholar
- Gordon CM, Baim S, Bianchi ML, et al. Special report on the 2007 Pediatric Position Development Conference of the International Society for Clinical Densitometry. South Med J. 2008; 101(7):740-743. PubMed | Google Scholar
- Mäyränpää MK, Helenius I, Valta H, Mäyränpää MI, Toiviainen-Salo S, Mäkitie O. Bone densitometry in the diagnosis of vertebral fractures in children: accuracy of vertebral fracture assessment. Bone. 2007; 41 (3):353-9. PubMed | Google Scholar
- Macdonald H, Kontulainen S, Petit M, Janssen P, McKay H. Bone strength and its determinants in pre- and early pubertal boys and girls. Bone. 2006 39(3):598-608. PubMed | Google Scholar
- Fricke O, Sumnik Z, Tutlewski B, Stabrey A, Remer T, Schoenau E. Local body composition is associated with gender differences of bone development at the forearm in puberty. Horm Res. 2008; 70(2):105-111. PubMed | Google Scholar
- Foley S, Quinn S, Jones G. Tracking of bone mass from childhood to adolescence and factors that predict deviation from tracking. Bone. 2009; 44(5):752-757. PubMed | Google Scholar
- Janicka A, Wren TA, Sanchez MM, et al. Fat mass is not beneficial to bone in adolescents and young adults. J Clin Endocrinol Metab. 2007;92(1):143-147. PubMed | Google Scholar
- Wang MC, Bachrach LK, Van Loan M, Hudes M, Flegal KM, Crawford PB. The relative contributions of lean tissue mass and fat mass to bone density in young women. Bone. 2005; 37(4): 474-481. PubMed | Google Scholar
- Reid IR. Relationships among body mass, its components, and bone. Bone. 2002;31(5):547-555. PubMed | Google Scholar
- Thomas T, Burguera B. Is leptin the link between fat and bone mass. J Bone Miner Res. 2002;17(9): 1563-1569. PubMed | Google Scholar
- akeda S, Elefteriou F, Levasseur R, Liu X, Zhao L, et al. Leptin regulates bone formation via the sympathetic nervous system. Cell. 2002;111(3):305-317. PubMed | Google Scholar
- Paulo G Pedreira, Marcelo M Pinheiro and Vera L Szejnfeld. Bone mineral density and body composition in postmenopausal women with psoriasis and psoriatic arthritis. Arthritis Res Ther. 2011 Feb 7;13(1):R16. PubMed | Google Scholar
- Högler W, Briody J, Moore B, Lu PW, Cowell CT. Effect of growth hormone therapy and puberty on bone and body composition in children with idiopathic short stature and growth hormone deficiency. Bone. 2005; 37(5):642-650. PubMed | Google Scholar
- Eley HL, Russell ST, Tisdale MJ. Mechanism of attenuation of muscle protein degradation induced by tumor necrosis factor-α and angiotensin II by ß-hydroxy-ß-methylbutyrate. Am J Physiol Endocrinol Metab. 2008 Dec;295(6):E1417-26. PubMed | Google Scholar
- Walsmith J, Roubenoff R. Cachexia in rheumatoid arthritis. Int J Cardiol. 2002; 85(1):89-99. PubMed | Google Scholar
- Mul D, van Suijlekom-Smit LW, ten Cate R, Bekkering WP, de Muinck Keizer-Schrama SM. Bone mineral density and body composition and influencing factors in children with rheumatic diseases treated with corticosteroids. J Pediatr Endocrinol Metab. 2002; 15(2):187-192. PubMed | Google Scholar
- Perez MD, Abrams SA, Loddeke L, Shypailo R, Ellis KJ. Effects of rheumatic disease and corticosteroid treatment on calcium metabolism and bone density in children assessed one year after diagnosis, using stable isotopes and dual energy x-ray absorptiometry. J Rheumatol. 2000; 27 (58):38-43. PubMed | Google Scholar
- Lien G, Selvaag AM, Flatø B, Haugen M, Vinje O, Sørskaar D, Dale K, Egeland T, Førre. A two-year prospective controlled study of bone mass and bone turnover in children with early juvenile idiopathic arthritis. Arthritis Rheum. 2005; 52(3): 833-840. PubMed | Google Scholar
- De Schepper J, Derde MP, Van den Broeck M, Piepsz A, et al. Normative data for lum¬bar spine bone mineral content in children: influ¬ence of age, height, weight, and pubertal stage. J Nucl Med. 1991;32(2): 216-220. PubMed | Google Scholar