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Rheumatology Advance Access originally published online on March 1, 2006
Rheumatology 2006 45(9):1125-1128; doi:10.1093/rheumatology/kel057
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© The Author 2006. Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Phalangeal bone ultrasound is of limited value in patients with juvenile idiopathic arthritis

I. Scheunemann1, G. E. Dannecker2 and J. Roth3,

1University Children's Hospital, 72076 Tübingen,2Department of Pediatrics and Pediatric Rheumatology, Olgahospital, 70176 Stuttgart and 3Pediatric Rheumatology, Charite Virchow Klinikum, 13353 Berlin, Germany.

Correspondence to: Johannes Roth, MD, SPZ Rheumatology, Charite Virchow Klinikum, Augustenburger Platz 1, 13353 Berlin, Germany. E-mail: johannes.roth{at}charite.de


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Discussion
 References
 
Objective. In children with juvenile idiopathic arthritis (JIA), alterations of the skeletal system have been described. The aim of this cross-sectional study was to evaluate a phalangeal bone ultrasound device in the assessment of the skeletal status in children with active JIA.

Methods. In 49 children with oligoarticular, polyarticular or systemic JIA, the speed of an ultrasound signal (Ad-SOS) through the phalanges of the dominant hand was measured using the Igea 1200.

Results. Children in all subgroups were significantly smaller than those in the reference population, but there were no significant deficits in Ad-SOS. The finger width was reduced only in patients with polyarticular JIA. The Ad-SOS correlated highly with height, but no correlation between the finger width and Ad-SOS, and no correlation between the standard deviation scores of body height and Ad-SOS were seen.

Conclusions. Phalangeal ultrasound is strongly dependent on body and therefore bone size, but other parameters of bone and soft tissues influence the measurements as well. It is not possible to differentiate as to which extent the various components of bone and soft tissue influence the measurement results. Ultrasound might therefore be of limited value in the assessment or screening of the skeletal system in children with JIA.

KEY WORDS: Juvenile idiopathic arthritis, Ultrasound, Bone, Musculoskeletal system.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Discussion
 References
 
Alterations of the skeletal system in children with juvenile idiopathic arthritis (JIA) have been described [1]. Until recently most studies assessing the bone status of children have been done using dual energy X-ray absorptiometry (DEXA) [2]. The DEXA technique has been questioned as the primary method of evaluating the skeletal status in these patients as it is very dependent on body size and cannot differentiate changes in bone density from alterations of bone geometry [3]. Quantitative CT measurements have been used to assess bone density of cortical and trabecular bone separately as well as geometric parameters of bone and muscle in children with rheumatic diseases [4]. Both methods have been criticized as they expose the patient to radiation, have not been available widely yet and are technically relatively challenging to perform. Ultrasound technology has been used as a radiation-free alternative with the potential advantage that results are influenced by bone density, microstructure, elasticity and geometry [5]. Different ultrasound devices have been developed that can be used to measure bone at various body sites (e.g. calcaneus, tibia and phalanges), some measuring the speed of the ultrasound signal (speed of sound, SOS), others measuring the attenuation of the signal (broadband ultrasound attenuation, BUA) or both. Previously published data in adults had shown a significant reduction of ultrasound velocity at the phalanges in patients with rheumatoid arthritis [6]. The aim of this study was to investigate whether ultrasound measurements at the phalanges in children with active JIA show alterations as compared with healthy controls and whether this technique might be useful for the assessment of the skeletal status in these children.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Discussion
 References
 
Subjects
Forty-nine patients seen regularly at the Pediatric Rheumatology Department of the Children's University Hospital in Tübingen, Germany, were studied. Twenty-five children had oligoarticular, 14 polyarticular and 10 systemic JIA. At the time of the measurements all patients had active disease defined by active arthritis and/or elevated C-reactive protein levels and erythrocyte sedimentation rates. Written informed consent was obtained from the parents according to the Declaration of Helsinki and the children agreed to take part. The study design was approved by the Ethics Committee of the University of Tübingen.

Study design
In this cross-sectional study, the patients received a physical examination including a complete joint assessment. Height and weight were recorded. All medication received at the time was documented. Ultrasound measurements of the fingers II–V of the dominant hand were performed as well as peripheral quantitative computed tomography (pQCT) measurements in 20 children.

Ultrasound measurements
The ultrasound velocity through the distal metaphysis of the proximal phalanx of the fingers was measured with a DBM Sonic 1200 (Igea, Carpi, Italy). The distance between the calipers (equalling the finger width) is measured and the time of flight calculated from the time the signal is generated to the time a certain voltage amplitude in the receiver is generated. The ultrasound velocity is calculated by dividing the finger width by the time of flight. Hence the SOS is amplitude-dependent and named Ad-SOS. The mean Ad-SOS of the fingers II–V of the dominant hand was compared separately with age- and height- matched reference data of 1328 healthy German children [7]. A standard deviation score (SDS) was calculated as:


Formula

The DBM Sonic was calibrated daily with a Plexiglas phantom. Studies had shown that, due to small differences in devices and phantoms, adjustments of the normative values need to be made for each machine [8]. With a single Plexiglas phantom test measurements were performed at five European institutions including our centre. The data were used to calculate corrected values for our machine. The precision of 10 in vivo measurements with repositioning for the same examiner was 0.31%. The inter-observer precision was 1.78% (data not shown). These results are comparable with previous studies [9].

Peripheral quantitative computed tomography
The pQCT measurements were performed using the XCT 2000 (Stratec Medizintechnik, Pforzheim, Germany) at the same time and the same arm as the ultrasound measurements. Measurements were taken at 4 and 66% of the forearm length. Patients’ results were compared with age-matched reference values resulting in a Z-score. A detailed description of the pQCT procedure including the references for the normative values is given in [4].

Statistical analysis
The 95% confidence intervals were calculated for the SDS-scores (ultrasound) or Z-scores (pQCT) of the patient data and the reference data. If there was no overlap between the two, differences were considered to be significant. For comparisons between the patient groups, the Mann–Whitney–Wilcoxon test (P<0.05) was used.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Discussion
 References
 
Characteristics of the study population and ultrasound results
The general data of the study population are shown in Table 1. Biometric data of the patients were compared with height and body mass index (BMI) data that had been recorded as part of the reference data study for the Igea 1200 [7]. Patients in all subgroups were significantly shorter than the reference population. Children with polyarticular JIA had a lower BMI and a smaller finger width. The results of the amplitude dependent SOS showed no significant changes compared with the reference population either by age or body height (Table 2). There was no significant difference between the age-matched and height-matched groups.


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  		TABLE 1. General data of the study population

 

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  		TABLE 2. Ad-SOS of the different patient groups

 
Influence of local arthritis and glucocorticoids
In order to investigate the influence of local arthritis, two groups with and without affected finger joints were compared (Table 2). Children with arthritic finger joints at the time of investigation had a smaller median Ad-SOS than children without affected finger joints when compared according to age, but a higher median Ad-SOS when compared according to body height. The difference between the groups was not significant.

As glucocorticoids are thought to exert major negative effects on bone metabolism, patients taking glucocorticoids were compared with patients without this medication (Table 2). The Ad-SOS was not significantly different between the two groups.

Influence of body height and finger width
Ad-SOS correlated with age (Pearson correlation coefficient R = 0.733, P<0.001) and height (R = 0.672, P<0.001) but the standard deviation of height did not correlate with the SDS of Ad-SOS, indicating that smaller children did not necessarily have lower ultrasound values. There was a significant correlation between the Ad-SOS and the finger width (R = 0.233, P = 0.012), but no significant correlation between the SDS of the Ad-SOS and the SDS of the finger width (R = –0.060, P = 0.084).

Comparison of ultrasound results with peripheral quantitative computed tomography
In 20 patients, a pQCT measurement had been taken at the time of the ultrasound measurement. For the comparison between ultrasound and pQCT, age-related reference values were taken. The median SDS (range) for trabecular density was –0.37 (–2.58 to 1.87), for cortical density 0.13 (–1.57 to 1.72) and for cortical area –0.91 (–3.3 to 0.52). Only the median SDS for cortical area was significantly different from the reference population (P<0.05). The corresponding ultrasound result in these 20 patients was a median (range) of Ad-SOS of 0.42 (–1.66 to 1.75).


   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
References
 
In this study, ultrasound measurements at the phalanges with the Igea 1200 could be performed with good precision. Great care was taken in the calibration of the ultrasound device and we took part in a cross calibration study among several institutions including the centre where the reference values had been obtained [8].

None of the JIA subgroups showed significant abnormalities in the Ad-SOS results. Arthritic finger joints did not result in significantly different Ad-SOS values of the phalanges either. This is in contrast to the results found in adults with rheumatoid arthritis [6]. An explanation might be that adults tend to develop periarticular bone loss leading to erosions faster than children. There was indeed a correlation of SOS values with Larsen stages in the adult population [6]. On the other hand, pQCT results, that were available in 20 of the children of our study, did show alterations of bone geometry (cortical area), whereas trabecular and cortical density were normal. These changes are similar to those described in a larger cohort of JIA patients [4] and indicate that the musculoskeletal system of the patients in this study was abnormal. These abnormalities were not detected by the ultrasound measurements.

The Ad-SOS results correlated with age, height and finger width. Ultrasound is strongly dependent on body/bone size and ultrasound values increase with age as well as with body height reflecting mainly an increase in bone size and not bone mineral density. In contrast, SDS for age and height did not correlate with the SDS of the ultrasound measurements, indicating that relatively smaller children did not necessarily have decreased ultrasound results. In fact, when we compared the patients’ results with height-matched reference values, the median SDS of our relatively smaller patients was higher than that in the comparison with age-matched reference values. It has to be noted though, that these comparisons suffer from several limitations: First, the soft tissue changes of arthritic finger joints in our patients might influence the measurements and therefore, add to the lack of correlation between SDS for height and SDS of Ad-SOS. Second, a comparison of the smaller JIA group to the height-matched reference group may result in an overestimation of bone health in JIA because, the children with JIA are being compared with younger children, possibly at earlier pubertal stages. These points nevertheless illustrate the main problem with ultrasound measurements of bone. It cannot be differentiated as to which extent abnormal values result from growth retardation, soft tissue changes, abnormal bone density or bone geometry and this might limit the use of phalangeal bone ultrasound especially in JIA patients.

It has been argued that weight-bearing bone and areas with a predominance of trabecular bone have to be studied to better detect changes in bone. The perfect location for this purpose would be the calcaneus. In one study, calcaneal BUA values and SDS in patients with JIA were significantly reduced as compared with controls both at baseline and follow-up [10]. It has to be noted though, that the children with JIA in this study were significantly smaller than the controls and that in a multiple regression analysis only body height was significant for changes in BUA over the 1 yr study period. In another study [11], a different ultrasound device was used to measure SOS at the distal radius and mid-shaft tibia. These data were compared with results obtained by DEXA at the lumbar spine. Again significantly reduced values were found in patients, but then again, these patients were significantly smaller than controls. The patient groups were also very heterogeneous. Interestingly, SOS at the tibia did not correlate strongly with body height.

Glucocorticoid therapy did not result in significantly different Ad-SOS values in our patients, but the number of patients was far too small for definitive statements. Morphologic changes of the bone during glucocorticoid therapy have been described to begin in trabecular bone [12]. Since the phalanges consist mostly of cortical bone, the alterations are expected to be less prominent at this site. Furthermore, low dose glucocorticoids do not necessarily affect the skeleton negatively [13].

Taken together, ultrasound measurements might well-respond to changes in bone but all the parameters available are only indirect estimates of density and structure. For a reliable assessment of bone in diseases like JIA, a separate and detailed determination of bone density and parameters of bone geometry is necessary.

Formula

The authors have declared no conflicts of interest.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 

  1. Mc Donagh. (2001) Osteoporosis in JIA. Curr Op Rheumatology 13:399–404.
  2. Pepmueller PH, Cassidy JT, Allen SH, Hillman LS. (1996) Bone mineralization and bone mineral metabolism in children with juvenile rheumatoid arthritis. Arthritis Rheum 39:746–57.[ISI][Medline]
  3. Schönau E. (1998) Problems of bone analysis in childhood and adolescence. Pediatr Nephrol 12:420–9.[CrossRef][ISI][Medline]
  4. Roth J, Palm C, Scheunemann I, Ranke MB, Schweizer R, Dannecker GE. (2004) Musculoskeletal abnormalities of the forearm in patients with juvenile idiopathic arthritis relate mainly to bone geometry. Arthritis Rheum 50:1277–85.[CrossRef][ISI][Medline]
  5. Gluer CC. International Quantitative Ultrasound Consensus Group. (1997) Quantitative ultrasound techniques for the assessment of osteoporosis: expert agreement on current status. J Bone Miner Res 12:1280–8.[CrossRef][ISI][Medline]
  6. Roeben P, Barkmann R, Ullrich S, Gause A, Heller M, Gluer CC. (2001) Assessment of phalangeal bone loss in patients with rheumatoid arthritis by quantitative ultrasound. Ann Rheum Dis 60:670–7.[Abstract/Free Full Text]
  7. Barkmann R, Rohrschneider W, Vierling M, Tröger J, et al. (2002) German pediatric reference data for quantitative transverse transmission ultrasound of finger phalanges. Osteoporosis Int 13:55–6.[Medline]
  8. Barkmann R and Glüer CC. (1998) Cross-calibration of the DBM Sonic 1200: quality assurance procedures for quantitative ultrasound measurements. Osteoporosis Int 8:Suppl. 3, 89–93.
  9. Soballa T, Wüster C, Schlegel J, et al. (1998) Ultrasound transmission speed and ultrasound bone profile score (UBPS) of the phalanges in normal women and women with osteoporosis. Horm Metab Res 30:536–41.[ISI][Medline]
  10. Falcini F, Bindi G, Simonini G, et al. (2003) Bone status evaluation with calcaneal ultrasound in children with rheumatic diseases. A one year follow up study. J Rheumatol 30:179–84.[ISI][Medline]
  11. Hartman C, Shamir R, Eshach-Adiv O, Iosilevsky G, Brik R. (2004) Assessment of osteoporosis by quantitative ultrasound versus Dual Energy X-ray absorptiometry in children with chronic rheumatic diseases. J Rheumatol 31:981–5.[ISI][Medline]
  12. Kotaniemi A, Savolainen A, Kautiainen H, Kroeger H. (1993) Estimation of central osteopenia in children with chronic polyarthritis treated with glucocorticoids. Pediatrics 91:1127–30.[Abstract/Free Full Text]
  13. Shibuya K, Hagino H, Morio Y, Teshima R. (2002) Cross-sectional and longitudinal study of osteoporosis in patients with rheumatoid arthritis. Clin Rheumatol 21:150–8.[CrossRef][ISI][Medline]
Submitted 11 August 2005; revised version accepted 27 January 2006.
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