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Prevalence of Vertebral Fractures in Children with Chronic Rheumatic

Diseases at Risk for Osteopenia
MERANDA NAKHLA, MD, FRCP(C), ROSIE SCUCCIMARRI, MD, FRCP(C), KAREN N. WATANABE DUFFY, MD, FRCP(C),
GAËLLE CHÉDEVILLE, MD, FRCP(C), SARAH CAMPILLO, MD, FRCP(C), CIARÁN M. DUFFY, MB BCH, FRCP(C),
E. MICHEL AZOUZ, MD, FRCP(C), NAZIH SHENOUDA, MD, FRCP(C), ATUL K. SHARMA, MD, FRCP(C), AND
CELIA RODD, MD, FRCP(C)

Objectives To determine the prevalence of and the risk factors for vertebral fractures in a cohort of children with chronic
rheumatic diseases considered at risk for osteopenia.
Study design We conducted a cross-sectional study of patients with chronic rheumatic diseases at the Montreal Children’s
Hospital.
Results Of the 90 study participants (22 boys, 68 girls), 10 boys and 7 girls (19%) were found to have vertebral fractures. These
17 children had a total of 50 fractures, an average of 2.9 per affected child. Fractures in the upper thoracic region (T5-8) accounted
for 55%. Only 56% of all fractures were symptomatic. With multivariate regression, we identified male sex (P < .01), body mass
index z-score (P < .02), and cumulative glucocorticoid dose (P < .01) as significant predictors of the number of vertebral fractures.
Conclusions Our study examined the prevalence of vertebral fractures in a high-risk pediatric population. Nineteen percent
of our cohort had vertebral fractures. Significant risk factors for the development of vertebral fractures include male sex and
cumulative glucocorticoid dose. Better understanding of the extent of the problem in this population will allow us to further
refine screening guidelines and treatment in these patients. (J Pediatr 2009;154:438-43)
steoporosis is a skeletal disorder characterized by low bone mass and deterioration of bone microarchitecture, resulting
in fragility fracture susceptibility. In children, low bone mass is caused by poor
bone accrual and ongoing bone loss caused by a number of factors. These
include inadequate calcium and vitamin D intake, chronic illness, limited weight-bearing
activity, medications, and hormonal imbalances. In adults, age-related fractures associated
From the Divisions of Endocrinology (M.N.,
with osteoporosis are a well-known entity, contributing to significant morbidity.1 In
C.R.), Rheumatology (R.S., K.W.D., G.C.,
children with chronic illnesses, osteoporosis, fragility fractures, and bone pain have
S.C., C.D.), and Nephrology (A.S.), Mon2-4
increasingly been recognized as a source of morbidity. However, the extent of this
treal Children’s Hospital, McGill University
Health Centre, Montreal, Quebec, Canada;
problem is poorly understood. Studies examining vertebral fractures in children have been
and Department of Radiology, Children’s
limited to case reports or have restricted their study population to children treated with
Hospital of Eastern Ontario, Ottawa, On4,5
tario, Canada (E.A., N.S.).
glucocorticoids or with low bone mineral density (BMD). Other studies have relied on
This project was funded by the Montreal
an indirect method of vertebral fracture identification by using dual-energy x-ray absorpChildren’s Hospital Research Institute. M.N.
tiometry (DXA) targeting scans, which have subsequently been invalidated by the authors
was funded by the Eli Lilly Canadian Pedi3-7
atric Endocrine Fellowship. The Montreal
themselves. A global assessment of children at risk of vertebral fractures is still lacking.
Children’s Hospital Research Institute did
Moreover, issues such as prevalence, risk factors, and natural history of vertebral fractures
not have a role in the development of the
study design, the collection, analysis, and
in children remain largely unknown.
interpretation of data, the writing of the
The rheumatology population is at particular risk for osteoporosis and fragility
report, or the decision to submit the paper
8-10
fractures because of the chronic inflammatory nature of the disease,
the medications
for publication. The authors declare no po11-13
tential conflicts of interest.
used to control disease activity, including glucocorticoids and methotrexate,
and the
14
Submitted for publication Jun 23, 2008; last
associated reduced physical activity and delayed puberty, which independently contribrevision received Aug 12, 2008; accepted
ute to fracture risk. We sought to determine the prevalence and predictors of vertebral
Sep 9, 2008.
Reprint requests: Meranda Nakhla, Division
fractures in this at-risk population by using plain thoracic and lumbar spine radiographs,

O

BMC
BMD
BMI
CTD
DXA

438

Bone mineral content
Bone mineral density
Body mass index
Connective tissue disease
Dual-energy x-ray absorptiometry

JDM
JIA
SLE
vBMD

Juvenile dermatomyositis
Juvenile idiopathic arthritis
Systemic lupus erythematosus
Volumetric BMD

of Endocrinology, Montreal Children’s Hospital, 2300 Tupper St, E-315, Montreal, Qc,
H3H 1P3, Canada. E-mail: nakhlam@yahoo.
com.
0022-3476/$ - see front matter
Copyright © 2009 Mosby Inc. All rights
reserved.
10.1016/j.jpeds.2008.09.023

From April 2005 to December 2006. and systemic vasculitis. A grading of 0. Carey. experts in reading pediatric vertebral fractures. including those with hyperthyroidism. independent predictors were the same variables used in the Poisson and multivariate regressions described below. we invited these children and adolescents who fulfilled criteria for being at risk for osteopenia and who were observed in the rheumatology clinic at Montreal Children’s Hospital to participate in the study. from which daily calcium (mg) and vitamin D (IU) intakes were calculated. These radiographs were read by 1 of 2 trained radiologists (E. Grade 0 corresponds to a normal vertebral body.15 We also set out to determine the predictors of low BMD. age of pubertal onset. We converted the glucocorticoid dosage to prednisone equivalency and also expressed this as prednisone per kg of body weight. including systemic lupus erythematosus (SLE) and juvenile dermatomyositis (JDM).18 allowing correction of the BMD for stature.which remain the radiographic gold standard. or N.19 The Mann-Whitney U test was used to test significance for median differences in baseline characteristics and risk factors between the fracture and non-fracture group. Two patients with vertebral fractures were missing dietary assessment of total daily calcium and vitamin D intake. a standardized food frequency questionnaire was administered to patients and their parents. At the same clinic visit. duration of disease. When there was a discrepancy. Both of these regression techniques were then applied to each of the imputed datasets. The heights were measured in triplicate. Genant scoring system for vertebral fractures. Parental informed consent and patient’s assent were obtained. Children as old as 18 years were included when they had earlier or current exposure to methotrexate. the films were Figure. re-read by the second pediatric radiologist. connective tissue disease (CTD). corticosteroids. the BMD was calculated excluding the affected vertebra(e). children were examined and Tanner staging was performed on all study subjects. Study participants and subjects who refused to participate were compared for age at diagnosis.17 All patients enrolled underwent plain lateral thoracic and lumbar spine radiography. Statistical analyses were performed with SAS software version 9. and diagnosis. associated diagnoses. parathyroid disorders. age and duration of disease at time of enrollment. and/or posterior height). When fractures involved the L2 to L4 region. who were blinded to the underlying diagnosis in the patients. Children with preexisting conditions that could affect calcium homeostasis were excluded. Also. and the results were formally pooled in SAS PROC MIANALYZE to provide unbiased parameter estimates that properly reflected the uncertainty associated with missing data. patients and parents were asked to complete a questionnaire about their personal and family history of fractures. For the imputation. We also determined the volumetric BMD (vBMD) for subjects ⬎7.M.15 The Genant scoring system assigns a score for each vertebra from T4 to L4 (Figure). North Carolina).). All study subjects also underwent BMD of the lumbar spine measured with the Hologic 4500A DXA. and the average was calculated. and other medical problems. we reviewed the charts of all patients observed in the rheumatology clinic at the Montreal Children’s Hospital and identified 113 individuals who met our inclusion criteria. METHODS In April 2005. grade 2 to a moderate fracture (26%-40% reduction in height). We used multivariate Poisson count regression analysis to identify pos- Prevalence of Vertebral Fractures in Children with Chronic Rheumatic Diseases at Risk for Osteopenia 439 . Each BMD was converted to a z-score by using the manufacturer’s standard pediatric reference range. Total lifetime exposure to oral and intravenous glucocorticoids was recorded. At the time of enrollment.16 In addition. Heights and weights were measured with a standard hospital scale and a Harpendon stadiometer. grade 1 to a mild fracture (20%-25% reduction in anterior. We reviewed the charts of the study subjects and extracted these characteristics: age at diagnosis.1 (SAS Institute. Heights and weights were converted to z-scores by using the Centers for Disease Control and Prevention-National Center for Health Statistics 2000 protocol.5 was used for minimal changes of the vertebral height or shape that did not fulfill criteria for Genant grade 1 and were considered normal variants. and grade 3 to a severe fracture (⬎40% reduction in height). either polyarthritis. osteoporosis. for which we performed multiple imputations with SAS PROC MI. A Genant score ⱖ1 was considered to be a definite compression fracture of the vertebral body. or psoriatic arthritis with ⱖ5 affected joints). missing values of total daily calcium and vitamin D intake were imputed (m ⫽ 10 replicates. The senior author reviewed all films. method ⫽ regression). middle. Vertebral fractures were graded on the basis of the semi-quantitative scoring method of Genant. extended oligoarthritis. or both and had the following diagnosis: juvenile idiopathic arthritis (JIA.5 years old and converted it to a z-score. and use of medications or supplements. In brief. systemic arthritis. we recorded the lifetime cumulative methotrexate doses in the form of mg per m2 of body surface area. malignancy. or primary bone disease.S.A.

L2. Except for exposure to long-term glucocorticoids (P ⬍ . In the steroid-naïve group. T7 T7. L3. there were no other significant differences seen in risk factors in the 2 groups. T6. T10. sible predictive factors for vertebral fractures. 1. and 1 psoriatic arthritis). Tables I and II). vBMD z-score (subjects ⬎7.5 years old and bone mineral content (BMC) were also examined as alternatives to the BMD z-score. 0. F. T8 T7 T11 T8. with a Genant score of 1. 1 polyarthritis arthritis. cumulative steroid dose per kg. 1 extended oligoarthritis. and 3 patients had not been exposed. T6. T7 T5. T11 T7. and BMC. Approximately 14% of the fractures were biconcave. disease duration. consisting of 22 boys and 68 girls.9 fractures per subject. Vertebral fractures were detected in 17 patients (19%). and 68% were anterior wedge. Male. The predictors included in the model were duration of disease. 14 patients had been exposed to steroids. Of the 17 children.1 years (range. L1. L3:L4 T7:T11 T11 T6 T6 2 4 2 T5. L3 T5. T11. Ethics approval was granted by the institutional review board at the Montreal Children’s Hospital. T8. total calcium and vitamin D intake. 18% were crush. We compared the baseline characteristics and risk factor variables between patients with and patients without vertebral fractures (Table II). T5.1 years). Tanner stage. More than half the fractures were symptomatic in the location of the fracture (56%). T8. with a score of 2.0 years). RESULTS Ninety-four of the 113 subjects who met the inclusion criteria agreed to participate in the study.Table I. and 3 patients had systemic vasculitis (Table I). and BMI z-score as significant independent predictors of vertebral fracture count (Table III). Body mass index (BMI)-z score. female. T11 T4. which included age at diagnosis. L4. the study participants.4-15. cumulative methotrexate dose in mg/m2. Vertebral fraction population Subjects Steroid treated 1 2 3 4 5 6 7 8 9 10 11 12 13 14 Steroid naïve 15 16 17 Sex Diagnosis M M M F M F M M M M F M F F Systemic vasculitis Systemic vasculitis Systemic vasculitis CTD-SLE CTD-SLE CTD-JDM CTD-JDM JIA–systemic JIA–systemic JIA–systemic JIA–systemic JIA–systemic JIA–psoriatic JIA–polyarthritis M F F JIA–polyarthritis JIA–extended oligoarthritis JIA–Psoriatic Number of vertebral fractures/Pain ⴝ* Location of vertebral fractures 2* 3 4 2* 1* 1* 4 3 11* 6 2* 1* 1* 1* L2. T7 T4:T5. sex.9-15. L5 T5:T6. corresponding to a loss of vertebral height of about 20% to 25%. L2. The Journal of Pediatrics • March 2009 .4-14. with a median duration of illness of 4. 4 subjects did not complete the radiography and were excluded from the analyses. In the group without vertebral fractures. 7 female. with a loss of height ⬎40%. In the steroid-treated group. with the remaining fractures occurring in the lumbar region. and lumbar spine BMD z-score. 35 patients (48%) were exposed to glucocorticoids. T10.3-18.03). had a median age of 13. We identified male sex. and sex. Two children had their vitamin D and calcium statuses imputed and were included in the analyses. The vBMD z-score for subjects ⬎7. cumulative prednisone dose in mg/kg.6 years (range. 8% of the fractures were moderate. a loss of height of 26% to 40%. 4. Multivariate linear regression was used to identify possible predictors of BMD. 0. 7 patients had JIA (5 systemic arthritis. T6 T7. T7. T6.7 years). cumulative dose of methotrexate per m2. including both dietary and supplemental sources. 1 psoriatic arthritis). cumulative glucocorticoid dosage per kg of body weight. The median age at diagnosis was 6. At the time of enrollment.5 years old). T7. age at diagnosis. data not shown).0 years (range. T9.7 years. The baseline characteristics between children who declined to participate or were excluded and children who participated were similar. 4 patients had CTD (2 SLE and 2 JDM). Fifty-five percent of the fractures were in the upper thoracic region of T4 to T8. Eightyeight percent of the fractures were mild.0 years (range. Of this group. averaging 2. with a slight predominance of male patients (10 male. Thoracic-region fractures comprised 78% of the vertebral fractures sustained. there were a total of 50 fractures.01) and BMI z-score (P ⫽ . all patients had JIA (1 polyarthritis. the median age at diagnosis 440 Nakhla et al was 7. T12. and 4% of the fractures were severe. although the pain was often transient and mild. L3 M.

BMI zscore. the mean total glucocorticoid dose (mg) was not found to be significantly different in the 2 groups.84 0.4) 336 (328-451) 1262 (1187-1511) *P value ⬍ .17-1. and lifetime glucocorticoid exposure (mg/kg). 56% 4.01* .08 . Male sex increased the expected number of vertebral fractures by a factor of 6. %) Median z-BMD (95% CI.7) 4.89 4.30-1.81). BMI z-score. The toxic effects of glucocorticoids on bone metabolism and calcium homeostasis are well known. either because of trauma or fragility fractures.4 However. or BMC were not found to increase vertebral fracture risk unless glucocorticoid exposure was omitted from the model.67-⫺0. we demonstrated a vertebral fracture prevalence of 19% in a high-risk general population of patients with rheumatic diseases.052.30 1.28).25 0.42-14.87-⫺0.49 (95% CI.5 (95% CI.62-1.16-0. most Prevalence of Vertebral Fractures in Children with Chronic Rheumatic Diseases at Risk for Osteopenia 441 .02 0.48 (⫺0.34 (0. n ⫽ 73) Median z-vBMD (95% CI) Median height z (95% CI) Median weight z (95% CI) Median BMI z (95% CI)* Median cumulative glucocorticoid dose (95% CI).6-3967.3-2748.04 1.4.60 (⫺0.08) when vBMD was included instead of BMD.40 (⫺2.17-1. earlier reports restricted their analyses to patients treated with glucocorticoids or with low BMD or used an unreliable indirect method of fracture identification.0 (0.5 (0.1) 5.31) ⫺0.55) 0.85-12.001* ⱕ. when these risks are multiplicative odds ratios. vBMD (n ⫽ 73 subjects).07) ⫺0.Table II.42-14.28 0.06-0. increased vertebral fracture risk was associated with male sex. 57% 22. 30% 9.09 0.9-15.34 (⫺0.33) 0. 13% ⫺0.61 (⫺2. Similarly.43) ⫺0.7) 42.6.76 ⬍. most fractures occurred in the upper thoracic region (T4-T8). After controlling for all the other factors in multivariate linear regression.09).17 (⫺0.10 0.36-0.89-1. This is in accordance with earlier pediatric studies that had found the thoracic region to be the most commonly affected site. IU Median total daily calcium intake (95% CI). Table III.01-⫺0.13 .50 0.25) 0.7) 1198. Mann-Whitney test.03-0.0 (873.3) 340 (296-507) 1183 (1068-1468) 73 12 M:61 F 6.34 (0.4-15. mg/m2 Median total daily vitamin D intake (95% CI). As was seen in our patients.37-12.9) 10. The relationship (collinearity) between glucocorticoids and bone mineralization is noteworthy because it suggests an explanation for the finding that BMD z-score is a significant predictor of vertebral fractures only when cumulative glucocorticoid dose is omitted from the model. reflecting a correlation in the 2 predictors (see linear regression results below). %) Systemic vasculitis (n.04 (95% CI.4-14.28 0. the z-scores for BMD. 16% ⫺1.1 (164.68-1.02* . DISCUSSION Literature on the prevalence of vertebral fractures in an unselected high-risk pediatric population with chronic rheumatic disease is limited.85-12. effectively adjusting the BMD for body size. 28% 3.49 1. and each 1 g/kg increase in cumulative glucocorticoid exposure increased the expected number of vertebral fractures by a factor of 4.17) 0.18 2. %) CTD (n. 1.09 0. Baseline characteristics of study population Characteristics Vertebral fracture No vertebral fractures n Sex distribution Median age at diagnosis (range).06 (⫺0.48) 258. 1.0 (1.38 *Statistically significant. In 3 separate multivariable regression models. and duration of disease were significant independent predictors of reduced BMD z-score (Table IV).98 0. These same factors were also found to be independent predictors of vBMD z-scores and of BMC (data not shown).0 (0.24 . unlike our study.4-674.46 2. years JIA (n.20 In our population of patients. Multivariate Poisson regression analysis for characteristics predicting vertebral fracture risk Characteristic Odds ratio 95% CI P value Sex (male) BMI z-score Duration of disease Age at diagnosis BMD z-score Cumulative glucocorticoid (g/kg) Cumulative methotrexate (g/m2) Total daily calcium intake (g) Total vitamin D intake (1000 IU) 6.82 . The strength of the association between fracture count and BMI z-score was considerably weaker (P ⫽ . years Median duration of illness (range). 2.56-0.05-2.19 (⫺1.60 (0. A case-control study examining the effect of prednisolone on vertebral fracture risk in children with juvenile chronic arthritis found that the mean daily dose of prednisolone (mg/kg) was significantly higher in those with vertebral fractures compared with those without fractures.21) ⫺0.3 (1693.81 1.5.94-1.0-116. mg/kg* Median cumulative methotrexate dose (95% CI). an increase in BMI z-score of 1 SD increased the expected fracture count by 1.17) 1.6-10.57 .4) 1584.5 In our study.05. cumulative glucocorticoid dosage. mg 17 10 M:7 F 7.

ethnicity.24 Furthermore.6 In addition.7 One hypothesis to explain the effect of male sex is that boys tend to be more involved in physical and risk-taking activities as compared with girls. this effect was not significant. increasing the expected risk of vertebral fractures by a factor of 6. in which 32 patients. potentially increasing their risk of physical injury. These factors may be affected even with a normal BMD result.064 0.3 There are several explanations for the lack of association between BMD measures and vertebral fracture risk. vBMD z-score.7 ⫻ 10⫺3 0.160 ⫺0.0045-0. Makitie et al devised a pediatric scoring system for the assessment of vertebral morphology.3 ⫻ 10⫺4 3. underwent spinal radiographs and lumbar BMD measurements. 3 had normal BMD z-scores. a retrospective cohort study of subjects with JIA reported a possible protective effect of disease modifying anti-rheumatic drugs including methotrexate on fracture risk.56 . a number of clinical variables confound BMD results.001 .5 In Makitie’s study. the Genant scoring method.8-10 The presence of tumor necrosis factor and interleukin-1 has been associated with suppression of osteoblast function and differentiation. Also. weight. We did not find BMD z-score.002-⫺0.0015 ⫺6.00 ⫺1. but not for bone thickness. of the 11 patients found to have vertebral fractures. decreasing bone formation. we did not use this scoring system because it has yet to be standardized. cumulative glucocorticoid dose was found to be a predictor of low BMD z-score. This finding raises the possible role of inflammatory cytokines in promoting bone fragility. this study was limited by its small sample size.52 P value .083 ⫺0. Thus. This is consistent with findings in a study conducted by Makitie et al.60 .6 ⫻ 10⫺4-3.001 ⫺1.5 ⫻ 10⫺3 ⫺0.3 However. has been found to be a risk factor for the development of vertebral fractures. it becomes difficult to distinguish their individual influences on the vertebral fracture count. fractures were in the upper thoracic region (T6-T8). DXA has its limitations in providing information on bone morphology and microarchitecture. lean body mass. and the results from Makitie’s study were released after our study had begun. glucocorticoid exposure. or BMC to be predictors of vertebral fractures. and after correction for bone size. and our results suggest that such corrections can explain at least part of the association between fractures and BMI described in this study and in the literature.0 ⫻ 10⫺4 1.3 However. because vertebrae in the mid-thoracic spine The Journal of Pediatrics • March 2009 . however.6 ⫻ 10⫺4 ⫺8. with various diagnoses and at risk of having 442 Nakhla et al secondary osteoporosis.04 ⬍. the results of BMD z-scores must be interpreted cautiously. was used. Helenius et al also noted an increased male preponderance of vertebral fractures in children after solid organ transplantation. Our study has several limitations. Literature on the effect of methotrexate on BMD and vertebral fractures is conflicting. although the underlying mechanism remains obscure.10 ⬍. in adults with rheumatic disorders. To date. including Tanner stage. With the inclusion of both independent variables into the Poisson regression model.061-0. including the existence of collinearity between the BMD z-score and cumulative prednisone dose.04.01 ß. however. One future direction will be to use the data collected to compare the Genant scoring method with the method devised by Makitie et al.43-0. Second. Predictors of BMD z-scores using multivariate linear regression analysis Explanatory variables ß Sex Male Female Total calcium intake (mg/day) Total vitamin D intake (IU/day) Age at diagnosis (years) Disease duration (years) Cumulative prednisone dose (mg/kg) Cumulative methotrexate dose (mg/m2) BMI z-score 0. Another pediatric study found a lack effect of glucocorticoids on vertebral fracture risk.Table IV.25 Correcting the BMD for height.9 We found male sex to be an independent predictor of vertebral fracture risk.8 ⫻ 10⫺4-⫺5. irrespective of diagnosis.22 Three of the patients who sustained vertebral fractures had not received steroids. other studies have demonstrated an association between BMD and vertebral fracture risk.5 Conversely.10 1. height.32 95% CI ⫺0.63 ⫺5.71 . We did not find methotrexate to have an effect on vertebral fracture risk or low BMD.4 ⫻ 10⫺5 0. as measured by mean daily dose.0 ⫻ 10⫺5 0. Further analyses will be conducted to clarify the clinical usefulness of these anthropometric corrections. which has only been standardized in adults.7 ⫻ 10⫺4-1. there are no standardized pediatric assessments of vertebral morphology. First.21.96 . A recent study by Reyes et al reported that methotrexate was an independent risk factor for vertebral fractures in children with rheumatic disorders in whom glucocorticoids are concomitantly prescribed. 8 were found to have normal BMD scores. As demonstrated in the linear regression analysis.23 Larger prospective studies may be required to delineate whether methotrexate is implicated in vertebral fracture risk or is protective because of its role in controlling inflammation. and BMI z-scores are strategies that can be used to increase the accuracy of BMD measurements.12-0. skeletal maturation. and bone size. because BMD corrects only for the area of bone studied. weight. Regression coefficients.

Capone A. J Pediatr 2005. King A.8:1137-48. As a result of this.17:1726-33. Bartolozzi G. Vinet AM.25:329-35. particularly because 44% of our fracture group was had no symptoms at the time of enrollment. Vertebral compression fractures in pediatric patients with Crohn’s disease.89:1484-8. population-based study. The primary role of steroids on the osteoporosis in juvenile rheumatoid patients evaluated by dual energy X-ray absorptiometry. Emerging insights into the pathophysiology of osteoporosis. Remes V. we did not request biochemical investigations because this may have lead to a decreased recruitment rate. Weinstein R. An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. 8. Bone densitometry in Canadian children 8-17 years of age. Peck SN. Junewick JJ. Desjardins LA. van Kuijk C. introduced selection bias.41:75-8. 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