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Ultrasound features of nonstructural lesions of the proximal and distal interphalangeal joints of the hands in patients with finger osteoarthritis
Joint Bone Spine 78 (2011) 65–69
Original article
Ultrasound features of nonstructural lesions of the proximal and distal interphalangeal joints of the hands in patients with finger osteoarthritis Stéphanie Arrestier ∗ , Carole Rosenberg , Fabien Etchepare , Sylvie Rozenberg , Violaine Foltz , Bruno Fautrel , Pierre Bourgeois Service de rhumatologie, hôpital Pitié-Salpêtrière, Assistance publique–Hôpitaux de Paris, 47, boulevard Hôpital, 75013 Paris, France
a r t i c l e
i n f o
Article history: Accepted 30 April 2010 Available online 4 July 2010 Keywords: Finger osteoarthritis Interphalangeal joints Ultrasonography
a b s t r a c t Objectives: To describe the ultrasound features of nonstructural damage (effusions, synovitis, Doppler signal abnormalities) in the proximal interphalangeal (PIP) and distal interphalangeal (DIP) joints of the fingers in patients with finger osteoarthritis compared to healthy controls. Methods: We included patients at a hospital-based outpatient rheumatology clinic who met American College of Rheumatology criteria for finger osteoarthritis and we compared them to healthy controls. Exclusion criteria were the same in both groups. We collected demographic data and symptoms. Ultrasonography (Esaote Technos machine, two sonographers) was performed in all participants in both groups and plain radiography in the patients only. The PIP and DIP joints on fingers 2 to 5 were evaluated. Ultrasound features were compared between the two groups. Results: We included 55 patients (51 women; 440 PIPs and 440 DIPs) and 46 healthy controls (368 PIPs and 368 DIPs). The rate of PIP joint effusion was similar in the two groups (patients, 2.05 ± 2.03; controls, 1.6 ± 1.7; P > 0.05), whereas the rate of DIP effusion was significantly higher in the patients (2.09 ± 1.87 versus 0 ± 0.6 in the controls; P < 0.05). Increased vascularization by Doppler evaluation was rare and occurred chiefly in the DIP joints of the patients. None of the participants in either group had synovitis. The ultrasound abnormalities were not significantly different between right- and left-handed individuals, and neither did they correlate with clinical disease expression or severity of the radiographic damage. © 2010 Published by Elsevier Masson SAS on behalf of the Société Française de Rhumatologie.
1. Introduction Finger osteoarthritis is a complex degenerative disease whose joint manifestations may be so intense as to suggest an inflammatory joint disease such as rheumatoid arthritis (RA) or psoriatic arthritis (PsA). Although the pathophysiology of finger osteoarthritis remains unclear, studies in knee osteoarthritis [1,2] suggest a key role for proinflammatory cytokines (IL-1 and TNF␣) in the development of the cartilage and bone lesions. Ultrasonography of the bones and joints is a valuable adjunct to the physical evaluation [3] and is widely used to diagnose and monitor inflammatory joint disease. In contrast, few studies have assessed the potential usefulness of ultrasonography in patients with osteoarthritis [4,5]. Detailed data on the nonstructural ultrasonography findings in patients with finger osteoarthritis would be useful in clinical practice and may provide pathophysiological insights. We investigated the ultrasound findings at the fingers in patients meeting American College of Rheumatology (ACR) crite-
∗ Corresponding author. Tel.: +33 1 42 17 78 05; fax: +33 1 42 17 79 59. E-mail address: [email protected] (S. Arrestier).
ria for finger osteoarthritis [6]. The objectives of our study were to describe nonstructural ultrasonography abnormalities in finger osteoarthritis, to establish the prevalence of these abnormalities comparatively with a population of healthy controls [7], and to evaluate correlations linking ultrasonography abnormalities to clinical symptoms and radiographic damage.
2. Methods 2.1. Patients Patients were recruited at the rheumatology outpatient clinic of a teaching hospital in Paris, France. The main reasons for patient visits were pain in the hands and functional impairment with joint stiffness. Patients were eligible if they met ACR criteria for finger osteoarthritis [6]. We did not include patients with any of the following: finger injury in the recent past, job requiring heavy manual labor, inflammatory joint disease, or crystal-induced arthropathy. Eligibility for the study was confirmed based on a medical history, physical evaluation, and review of plain radiographs of the hands obtained within the past year.
1297-319X/$ – see front matter © 2010 Published by Elsevier Masson SAS on behalf of the Société Française de Rhumatologie. doi:10.1016/j.jbspin.2010.05.006
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S. Arrestier et al. / Joint Bone Spine 78 (2011) 65–69
Table 1 Clinical features in the patients with finger osteoarthritis and the healthy controls.
Sex, n Mean age in years (range) Handedness, n Mean symptom duration in months (range) Time-course
F M Right Left Flares (n/%) Continuous (n/%) Flares + Continuous (n/%)
Dreiser algofunctional index
For each patient, we collected the following data: age, sex, occupation, handedness, time-course of symptoms (continuous, flares, or both), joints tender spontaneously and upon squeezing, visual analog scale (VAS) score for overall pain, and Dreiser angofunctional index (DAFI) [8]. A flare was defined as joint pain, either spontaneously or upon squeezing, with swelling. Plain radiographs of the hands were obtained if none taken within the last year were available for review. Each radiograph was read by the two main investigators, who were unaware of the ultrasonography results, to rule out inflammatory or crystal-induced joint disease and to determine the modified Kellgren-Lawrence score [9]. 2.2. Controls The healthy controls were recruited for another study [7]. Inclusion criteria were age younger than 40 years, absence of symptoms in the hands or fingers, negative history for finger injury, and no heavy manual labor. We used a population of young controls to minimize the rate of asymptomatic finger osteoarthritis in the control group. 2.3. Ultrasonography In all patients and controls, ultrasonography was performed using an Esaote (Technos MP) machine and a 10–13 MHz linear array transducer. In each patient, ultrasonography was performed by two sonographers (SA and CR) who worked together to reach a consensus about the findings. Both sonographers were rheumatologists with theoretical and practical training in osteoarticular ultrasonography (EULAR online course and Paris VI ECHORHUM university diploma) and over 2 years of experience with osteoarticular ultrasonography in clinical practice. In each patient and control, the proximal interphalangeal (PIP) and distal interphalangeal (DIP) joints of digits 2 to 5 of both hands were examined using the standard ultrasonography method recommended by the EULAR. The volar and palmar aspects of the joints were scanned longitudinally. Power Doppler imaging was performed using a frequency of 8.3 MHz and a pulse repetition frequency of 750 MHz. B-mode images were examined for joint effusion, synovitis, and flexor tenosynovitis. Joint effusion and synovitis were defined according to OMERACT criteria [10] (echo-free zone for joint effusion and intracapsular hypoechogenic zone for synovitis). Joint effusions were measured on the palmar view; the greatest distance from the bone to the capsule was measured (mm) on the proximal side, perpendicularly to the diaphysis. However, joint effusions located under the flexor tendons were recorded but not measured. Joint effusions were described using a quantitative score derived from Szkudlarek’s score [3], as follows: 0, no effusion; 1, effusion under the tendon; 2, moderate effusion without distension of the joint capsule; and 3, large effusion with distension of the capsule. On power Doppler images, inflammation was scored semi-quantitatively from 0 to 3. Structural lesions were not evalu-
Patients (n = 55)
Controls (n = 46)
51 4 61.4 (51–89) 54 1 60 (4–360) 29/52.7 13/23.64 13/23.63 8.03 ± 5.5
33 13 25.5 (18–39) 41 5
ated. We did not assess the metacarpophalangeal joints, which are less affected by osteoarthritis. 3. Statistical analysis Statistical analyses were done using Stata® Release 5 Software (College Station, TX, USA). P values smaller than 0.05 were considered statistically significant. Differences in joint effusion distribution between patients and controls were assessed using the chi-square test or, when sample sizes were small, the Fisher exact test. In the patients, potential correlations linking ultrasonography findings to clinical manifestations and radiographic lesion severity were assessed by computing the kappa coefficient. 4. Results We included 55 patients with symptomatic finger osteoarthritis between August and December 2006. There were 51 (93%) women and four men with a mean age of 61.4 years (range, 51–89) and mean symptom duration of 5 years (range, 4–360 months). Among them, 54 (98%) were right-handed. The time-course profile was a succession of flares and remissions in 29 (52.7%) patients, continuous pain in 13 (23.6%) and continuous pain with flares in 13 (23.6%). Mean DAFI was 8.03 ± 5.5 (range, 0–21) indicating mild disease (maximum score, 30). At the time of the study, a clinical flare was ongoing for 66 PIP and 46 DIP joints (Table 1). The clinical and ultrasonography features in the 46 healthy controls have been described elsewhere [7]. There were 33 (71.7%) women and 13 men with a mean age of 25.5 years (range, 18–39). Among them, 41 (89%) were right-handed (Table 1). We compared the ultrasound features of the 440 PIP and 440 DIP joints in the patients to those in the 368 PIP and 368 DIP joints in the controls. 4.1. Distribution of ultrasound abnormalities in the patients with finger osteoarthritis 4.1.1. Intracapsular effusions of the proximal interphalangeal joints Of the 440 PIP joints in the patients, 113 (25.7%) showed effusions. Mean effusion size was 1.04 ± 0.3 mm and mean number of Table 2 Distribution of intracapsular effusions in the proximal and distal interphalangeal joints of each hand in the patients with finger osteoarthritis. Ray
Dominant hand Nondominant hand
PIP DIP PIP DIP
Total
2
3
4
5
11 14 10 15
15 23 15 19
15 15 20 8
16 13 11 8
PIP: proximal interphalangeal joints; DIP: distal interphalangeal joints.
57 65 56 50
S. Arrestier et al. / Joint Bone Spine 78 (2011) 65–69
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effusions per patient (counting both sides) was 2.05 ± 2.03. The PIP joint effusions were evenly distributed between the dominant and nondominant side, as well as among the four fingers studied on each side (Table 2). 4.1.2. Intracapsular effusions of the distal interphalangeal joints Of the 440 DIP joints, 115 (26%) showed effusions. Mean effusion size was 1.15 ± 0.5 mm and mean number of effusions per patient (both sides) was 2.09 ± 1.87. The DIP joint effusions were evenly distributed between the dominant and nondominant side, as well as among the four fingers studied on each side (Table 2). 4.1.3. Subtendinous effusions Overall subtendinous effusions were seen in 107 (24.2%) PIP joints and one DIP joint. On the dominant side, subtendinous effusions were seen in 60 PIP and zero DIP joints; corresponding figures on the nondominant side were 47 and one. The subtendinous effusions were evenly distributed between the dominant and nondominant side but preferentially affected the third PIP joint (21.3% on the dominant side and 19.5% on the nondominant side). 4.1.4. Synovitis None of the PIP or DIP joints in the patients with finger osteoarthritis showed evidence of synovitis. 4.1.5. Power Doppler imaging Joints with intracapsular or subtendinous effusions were examined using power Doppler imaging to look for hypervascularization. Of the 440 PIP joints, three showed grade 1 signals and one showed a grade 2 signal. Of the 440 DIP joints, 15 showed grade 1 signals and one showed a grade 3 signal; these signals were distributed evenly between the dominant and nondominant sides but preferentially affected the second DIP (n = 6) and third DIP (n = 8) joints. The power Doppler signals were typical for inflammation and did not suggest physiological vascularization (Fig. 1). 4.2. Comparison of ultrasound findings between patients and controls For intracapsular effusions of the PIP joints, no statistically significant differences were found between the patients and the controls (Fisher’s exact test, P > 0.05) (Table 3). In contrast, intracapsular effusions of the DIP joints were significantly more common in the patients than in the controls (P < 0.05) (Table 4). For subtendinous effusions in the PIP joints, no statistically significant differences were found between the patients and the controls (Fisher’s exact test, P > 0.12 for all PIPs, on the dominant and nondominant sides). A single subtendinous effusion was found in a DIP joint, which precluded a statistical evaluation of this feature. Similarly, the small number of Doppler signals in the patients and absence of Doppler signals in the controls precluded a meaningful statistical evaluation. However, it is interesting to note that hypervascularization, although rare, can occur in finger osteoarthritis and is then usually seen as a low-grade signal.
Fig. 1. a: ultrasonography abnormalities in finger osteoarthritis; b: palmar view showing an intracapsular effusion and an osteophyte, with no Doppler signal; c: palmar view showing an effusion and a grade 3 Doppler signal.
4.3. Correlations In the patients with finger osteoarthritis, we looked for correlations linking the ultrasonography findings to the clinical and radiographic manifestations, by computing the kappa coefficients. Clinical flares were not significantly correlated with presence of an intracapsular effusion by ultrasonography (Ä = 0.14) or a positive Doppler signal (Ä = 0.06). Neither were radiographic changes correlated with presence of an intracapsular effusion by ultrasonography (Ä = 0.03) or a positive Doppler signal (Ä = 0.0105). 5. Discussion Ultrasonography was recently investigated as a tool for evaluating osteoarthritis [4,5]. However, few studies have focused on ultrasonography findings in osteoarthritis of the hands. In 2007, 15 experts conducted a systematic literature review [11], which identified only two relevant studies [12,13]. The objective of the study was to develop a preliminary ultrasonographic scoring system for hand osteoarthritis. In each of seven patients, 15 joints of the dominant hand were examined (five metacarpophalangeal joints, five PIP joints, four DIP joints and the thumb metacarpophalangeal joint). Synovial hypertrophy and joint effusions were assessed using OMERACT criteria [10]. Power Doppler signals and osteophytes were also recorded. Intraobserver and interobserver
Table 3 Intracapsular effusions in the proximal and distal interphalangeal joints in the patients with finger osteoarthritis and in the healthy controls. PIP
Effusion (n/%) Effusion size in mm, mean ± SD Number of effusions/patient, mean ± SD Doppler signal (n/%)
DIP
Patients
Controls
Patients
Controls
113/25.7 1.04 ± 0.3 2.05 ± 2.03 4/3.5
77/21 0.83 ± 0.25 1.6 ± 1.7 0
115/26 1.15 ± 0.5 2.09 ± 1.87 16/13.9
11/2.1 0.72 ± 0.16 0 ± 0.6 0
PIP: proximal interphalangeal joints; DIP: distal interphalangeal joints.
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S. Arrestier et al. / Joint Bone Spine 78 (2011) 65–69
Table 4 Distribution of intracapsular effusions in the distal interphalangeal joints in patients with finger osteoarthritis and in healthy controls. DIP 2
Dominant hand Nondominant hand
DIP 3
DIP 4
DIP 5
OA
C
OA
C
OA
C
OA
C
14 P < 0.01 15 P < 0.01
0
23 P < 0.01 19 P < 0.01
2
15 P = 0.047 8 P = 0.106
5
13 P = 0.003 8 P = 0.007
1
0
1
2
0
DIP: distal interphalangeal joint; OA: patient with finger osteoarthritis; C: healthy control.
correlation coefficients were acceptable for these three features. These preliminary results suggest that ultrasonography may hold promise for evaluating osteoarthritis and provide a basis for developing an ultrasonography score [11]. More recently, a study of 1106 joints in 37 patients with hand osteoarthritis compared ultrasonography and standard radiography for evaluating the joint spaces and detecting osteophytes at the fingers [14]. Erosions were not studied. Compared to standard radiography, ultrasonography performed better for detecting osteophytes (Ä = 0.54) and metacarpophalangeal joint space narrowing [14]. We described nonstructural abnormalities (synovial hypertrophy, effusions, and Doppler signal) in patients with finger osteoarthritis. Osteophytes and erosions were not investigated. Erosions are difficult to detect by ultrasonography in fingers with osteoarthritis, both because they develop chiefly within bones and because they are often concealed by osteophytes. Furthermore, in everyday practice, the most common problem is the diagnosis of early osteoarthritis, often before the development of structural changes. We used a group of healthy controls to detect differences between normal and abnormal ultrasonography findings. We decided to use controls not older than 40 years of age to minimize the rate of undiagnosed asymptomatic osteoarthritis lesions in the control group. The absence of matching of the controls to the patients on age and sex may have introduced a bias, as the rates of synovial hypertrophy and joint effusions may vary with age and sex. However, a recent study of ultrasonography findings in patients with symptomatic finger osteoarthritis and in age- and sex-matched controls found significantly larger numbers of abnormalities in the patients [15]. The discrepancies between this study [15] and ours may be related to the exclusion from our study of structural changes (joint space narrowing and osteophytes) and of the metacarpophalangeal, carpometacarpal, and thumb PIP joints. However, the osteoarthritis changes predominantly affected the DIP joints. In our study, the number of effusions at the PIPs was not greater in the patients than in the controls, although the effusions were slightly larger (1.04 ± 0.3 mm versus 0.83 ± 0.25 mm). An ultrasonography study of patients with rheumatoid arthritis showed an increase in synovial thickness at the PIP joints compared to healthy controls (1.25 ± 0.87 mm versus 0.38 ± 0.34 mm), the optimal cutoff for distinguishing normal from abnormal PIP joints being 0.6 mm [16]. In our study, the only statistically significant difference between the patients and the controls was a higher rate of DIP joint effusions in the patients. Again, the size of these effusions seemed greater in the patients. A study in 15 patients with PsA and five with RA, as well as in five healthy controls, compared ultrasonography to standard radiography and magnetic resonance imaging [17]. Ultrasonography detected a larger number of DIP joint abnormalities in the PsA patients than in the RA patients or controls, but these lesions consisted chiefly in bone proliferation rather than in synovial hypertrophy, which was seen in 22% of DIP joints in the PsA group compared to 23% in the RA group and 3% in
the control group. Power Doppler imaging was not performed [17]. A large number of PIP joints in our study exhibited subtendinous effusions at the palmar side, with no difference between patients and controls. As pointed out in our previous study [7], the meaning of these effusions is unclear. Power Doppler imaging indicated hypervascularization of four PIP and 16 DIP joints in our patients and none of our controls. The small number of joints with hypervascularization precluded a statistical evaluation. Thus, further investigation of this feature is needed. In a group of patients with erosive finger osteoarthritis, power Doppler imaging showed a considerably higher rate of hypervascularization (22.4% of joints) [18]. However, another study of patients with finger osteoarthritis found no correlation between presence of a clinical flare and presence of an intracapsular effusion with or without a power Doppler signal [15]. Our study indicates that the main differences in nonstructural lesions between healthy individuals and patients with finger osteoarthritis are found at the DIP joints. Effusions in the PIP joints do not seem to reliably indicate disease. To better delineate the ultrasonography features of the PIP joints, a comparison with RA patients would be of interest. For the DIP joints, comparing the ultrasonography findings to those in patients with PsA may prove useful. Finally, in both the patients and the healthy controls, and at both the PIP joints and the DIP joints, the abnormalities were usually seen at the palmar aspect of the fingers. In patients with pain and swelling of the PIP and DIP joints, ultrasonography delineates the lesions, providing objective data for distinguishing between inflammatory joint disease and osteoarthritis. Available studies suggest a key diagnostic role for ultrasonography, most notably in doubtful cases.
Conflict of interest statement The authors have no conflict of interest to declare.
References [1] Ayral X, Pickering EH, Woodworth TG, et al. Synovitis: a potential predictive factor of structural progression of medial tibiofemoral knee osteoarthritis-results of a 1-year longitudinal arthroscopic study in 422 patients. Osteoarthritis Cartilage 2005;13:361–7. [2] Hill CL, Hunter DJ, Niu J, et al. Synovitis detected on magnetic resonance imaging and its relation to pain and cartilage loss in knee osteoarthritis. Ann Rheum Dis 2007;66:1599–603. [3] Szkudlarek M, Court-Payen M, Jacobsen S, et al. Interobserver agreement in ultrasonography of the finger and toe joint in rheumatoid arthritis. Arthritis Rheum 2003;48:955–62. [4] D’Agostino MA, Conaghan P, Le Bars M, et al. EULAR report on the use of ultrasonography in painful knee osteoarthritis Part 1: prevalence of inflammation in osteoarthritis. Ann Rheum Dis 2005;64:1703–9. [5] Naredo E, Cabero F, Palop MJ, et al. Ultrasonographic findings in knee osteoarthritis: a comparative study with clinical and radiographic assessment. Osteoarthritis cartilage 2005;13:568–74. [6] Altman R, Alarcon G, Appelrouth D, et al. The American Rheumatology criteria for the classification and reporting of osteoarthritis of the hand. Arthritis Rheum 1990;33:1601–10.
S. Arrestier et al. / Joint Bone Spine 78 (2011) 65–69 [7] Rosenberg C, Arrestier S, Etchepare F, et al. High frequency of ultrasonographic effusion in interphalangeal joints of healthy subjects: a descriptive study. Joint Bone Spine 2009;76:265–7. [8] Dreiser RL, Maheu E, Guillou GB, et al. Validation of an algofunctional index for osteoarthritis of the hand. Rev Rhum Engl Ed 1995 Jun;62(6 Suppl 1):43S–53S. [9] Dahaghin S, Bierma-Zeinstra SM, Ginai AZ, et al. Prevalence and pattern of radiographic hand osteoarthritis and association with pain and disability (the Rotterdam study). Ann Rheum Dis 2005;64:682–7. [10] Wakefield RJ, Balint PV, Szkudlarek M, et al. OMERACT Special Interest Group Musculoskeletal ultrasound including definitions for ultrasonographic pathology. J Rheumatol 2005;32:2485–7. [11] Keen HI, Lavie F, Wakefield RJ, et al. The development of a preliminary ultrasonographic scoring system for features of hand osteoarthritis. Ann Rheum Dis 2008;67:651–5. [12] Iagnocco A, Filippucci E, Ossandon A, et al. High resolution ultrasonography in detection of bone erosions in patients with hand osteoarthritis. J Rheumatol 2005;32:2381–3. [13] Iagnocco A, Coari G. Usefulness of high resolution US in the evaluation of effusion in osteoarthritic first metacarpal joint. Scand J Rheumatol 2000;29:170–3.
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[14] Keen HI, Wakefield RJ, Grainger AJ, et al. Can ultrasonography improve on radiographic assessment in osteoarthritis of the hands? A comparison between radiographic and ultrasonographic detected pathology. Ann Rheum Dis 2008;67:1116–20. [15] Keen HI, Wakefield RJ, Grainger AJ, et al. An ultrasonography study of osteoarthritis of the hand: synovitis and its relationship to structural pathology and symptoms. Arthritis Rheum 2008;59(12):1756–63. [16] Scheel AK, Hermann KG, Kahler E, et al. A novel ultrasonographic synovitis scoring system suitable for analyzing finger joint inflammation in rheumatoid arthritis. Arthritis Rheum 2005;52:733–43. [17] Wiell C, Szkudlarek M, Hasselquist M, et al. Ultrasonography, magnetic resonance imaging, radiography and clinical assessment of inflammatory and destructive changes in fingers and toes of patients with psoriatic arthritis. Arthritis Res Ther 2007;9:R119. [18] Vlychou M, Koutroumpas A, Malizos K, et al. Ultrasonographic evidence of inflammation is frequent in hands of patients with erosive osteoarthritis. Osteoarthritis Cartilage 2009;17:1283–7.
Original article
Ultrasound features of nonstructural lesions of the proximal and distal interphalangeal joints of the hands in patients with finger osteoarthritis Stéphanie Arrestier ∗ , Carole Rosenberg , Fabien Etchepare , Sylvie Rozenberg , Violaine Foltz , Bruno Fautrel , Pierre Bourgeois Service de rhumatologie, hôpital Pitié-Salpêtrière, Assistance publique–Hôpitaux de Paris, 47, boulevard Hôpital, 75013 Paris, France
a r t i c l e
i n f o
Article history: Accepted 30 April 2010 Available online 4 July 2010 Keywords: Finger osteoarthritis Interphalangeal joints Ultrasonography
a b s t r a c t Objectives: To describe the ultrasound features of nonstructural damage (effusions, synovitis, Doppler signal abnormalities) in the proximal interphalangeal (PIP) and distal interphalangeal (DIP) joints of the fingers in patients with finger osteoarthritis compared to healthy controls. Methods: We included patients at a hospital-based outpatient rheumatology clinic who met American College of Rheumatology criteria for finger osteoarthritis and we compared them to healthy controls. Exclusion criteria were the same in both groups. We collected demographic data and symptoms. Ultrasonography (Esaote Technos machine, two sonographers) was performed in all participants in both groups and plain radiography in the patients only. The PIP and DIP joints on fingers 2 to 5 were evaluated. Ultrasound features were compared between the two groups. Results: We included 55 patients (51 women; 440 PIPs and 440 DIPs) and 46 healthy controls (368 PIPs and 368 DIPs). The rate of PIP joint effusion was similar in the two groups (patients, 2.05 ± 2.03; controls, 1.6 ± 1.7; P > 0.05), whereas the rate of DIP effusion was significantly higher in the patients (2.09 ± 1.87 versus 0 ± 0.6 in the controls; P < 0.05). Increased vascularization by Doppler evaluation was rare and occurred chiefly in the DIP joints of the patients. None of the participants in either group had synovitis. The ultrasound abnormalities were not significantly different between right- and left-handed individuals, and neither did they correlate with clinical disease expression or severity of the radiographic damage. © 2010 Published by Elsevier Masson SAS on behalf of the Société Française de Rhumatologie.
1. Introduction Finger osteoarthritis is a complex degenerative disease whose joint manifestations may be so intense as to suggest an inflammatory joint disease such as rheumatoid arthritis (RA) or psoriatic arthritis (PsA). Although the pathophysiology of finger osteoarthritis remains unclear, studies in knee osteoarthritis [1,2] suggest a key role for proinflammatory cytokines (IL-1 and TNF␣) in the development of the cartilage and bone lesions. Ultrasonography of the bones and joints is a valuable adjunct to the physical evaluation [3] and is widely used to diagnose and monitor inflammatory joint disease. In contrast, few studies have assessed the potential usefulness of ultrasonography in patients with osteoarthritis [4,5]. Detailed data on the nonstructural ultrasonography findings in patients with finger osteoarthritis would be useful in clinical practice and may provide pathophysiological insights. We investigated the ultrasound findings at the fingers in patients meeting American College of Rheumatology (ACR) crite-
∗ Corresponding author. Tel.: +33 1 42 17 78 05; fax: +33 1 42 17 79 59. E-mail address: [email protected] (S. Arrestier).
ria for finger osteoarthritis [6]. The objectives of our study were to describe nonstructural ultrasonography abnormalities in finger osteoarthritis, to establish the prevalence of these abnormalities comparatively with a population of healthy controls [7], and to evaluate correlations linking ultrasonography abnormalities to clinical symptoms and radiographic damage.
2. Methods 2.1. Patients Patients were recruited at the rheumatology outpatient clinic of a teaching hospital in Paris, France. The main reasons for patient visits were pain in the hands and functional impairment with joint stiffness. Patients were eligible if they met ACR criteria for finger osteoarthritis [6]. We did not include patients with any of the following: finger injury in the recent past, job requiring heavy manual labor, inflammatory joint disease, or crystal-induced arthropathy. Eligibility for the study was confirmed based on a medical history, physical evaluation, and review of plain radiographs of the hands obtained within the past year.
1297-319X/$ – see front matter © 2010 Published by Elsevier Masson SAS on behalf of the Société Française de Rhumatologie. doi:10.1016/j.jbspin.2010.05.006
66
S. Arrestier et al. / Joint Bone Spine 78 (2011) 65–69
Table 1 Clinical features in the patients with finger osteoarthritis and the healthy controls.
Sex, n Mean age in years (range) Handedness, n Mean symptom duration in months (range) Time-course
F M Right Left Flares (n/%) Continuous (n/%) Flares + Continuous (n/%)
Dreiser algofunctional index
For each patient, we collected the following data: age, sex, occupation, handedness, time-course of symptoms (continuous, flares, or both), joints tender spontaneously and upon squeezing, visual analog scale (VAS) score for overall pain, and Dreiser angofunctional index (DAFI) [8]. A flare was defined as joint pain, either spontaneously or upon squeezing, with swelling. Plain radiographs of the hands were obtained if none taken within the last year were available for review. Each radiograph was read by the two main investigators, who were unaware of the ultrasonography results, to rule out inflammatory or crystal-induced joint disease and to determine the modified Kellgren-Lawrence score [9]. 2.2. Controls The healthy controls were recruited for another study [7]. Inclusion criteria were age younger than 40 years, absence of symptoms in the hands or fingers, negative history for finger injury, and no heavy manual labor. We used a population of young controls to minimize the rate of asymptomatic finger osteoarthritis in the control group. 2.3. Ultrasonography In all patients and controls, ultrasonography was performed using an Esaote (Technos MP) machine and a 10–13 MHz linear array transducer. In each patient, ultrasonography was performed by two sonographers (SA and CR) who worked together to reach a consensus about the findings. Both sonographers were rheumatologists with theoretical and practical training in osteoarticular ultrasonography (EULAR online course and Paris VI ECHORHUM university diploma) and over 2 years of experience with osteoarticular ultrasonography in clinical practice. In each patient and control, the proximal interphalangeal (PIP) and distal interphalangeal (DIP) joints of digits 2 to 5 of both hands were examined using the standard ultrasonography method recommended by the EULAR. The volar and palmar aspects of the joints were scanned longitudinally. Power Doppler imaging was performed using a frequency of 8.3 MHz and a pulse repetition frequency of 750 MHz. B-mode images were examined for joint effusion, synovitis, and flexor tenosynovitis. Joint effusion and synovitis were defined according to OMERACT criteria [10] (echo-free zone for joint effusion and intracapsular hypoechogenic zone for synovitis). Joint effusions were measured on the palmar view; the greatest distance from the bone to the capsule was measured (mm) on the proximal side, perpendicularly to the diaphysis. However, joint effusions located under the flexor tendons were recorded but not measured. Joint effusions were described using a quantitative score derived from Szkudlarek’s score [3], as follows: 0, no effusion; 1, effusion under the tendon; 2, moderate effusion without distension of the joint capsule; and 3, large effusion with distension of the capsule. On power Doppler images, inflammation was scored semi-quantitatively from 0 to 3. Structural lesions were not evalu-
Patients (n = 55)
Controls (n = 46)
51 4 61.4 (51–89) 54 1 60 (4–360) 29/52.7 13/23.64 13/23.63 8.03 ± 5.5
33 13 25.5 (18–39) 41 5
ated. We did not assess the metacarpophalangeal joints, which are less affected by osteoarthritis. 3. Statistical analysis Statistical analyses were done using Stata® Release 5 Software (College Station, TX, USA). P values smaller than 0.05 were considered statistically significant. Differences in joint effusion distribution between patients and controls were assessed using the chi-square test or, when sample sizes were small, the Fisher exact test. In the patients, potential correlations linking ultrasonography findings to clinical manifestations and radiographic lesion severity were assessed by computing the kappa coefficient. 4. Results We included 55 patients with symptomatic finger osteoarthritis between August and December 2006. There were 51 (93%) women and four men with a mean age of 61.4 years (range, 51–89) and mean symptom duration of 5 years (range, 4–360 months). Among them, 54 (98%) were right-handed. The time-course profile was a succession of flares and remissions in 29 (52.7%) patients, continuous pain in 13 (23.6%) and continuous pain with flares in 13 (23.6%). Mean DAFI was 8.03 ± 5.5 (range, 0–21) indicating mild disease (maximum score, 30). At the time of the study, a clinical flare was ongoing for 66 PIP and 46 DIP joints (Table 1). The clinical and ultrasonography features in the 46 healthy controls have been described elsewhere [7]. There were 33 (71.7%) women and 13 men with a mean age of 25.5 years (range, 18–39). Among them, 41 (89%) were right-handed (Table 1). We compared the ultrasound features of the 440 PIP and 440 DIP joints in the patients to those in the 368 PIP and 368 DIP joints in the controls. 4.1. Distribution of ultrasound abnormalities in the patients with finger osteoarthritis 4.1.1. Intracapsular effusions of the proximal interphalangeal joints Of the 440 PIP joints in the patients, 113 (25.7%) showed effusions. Mean effusion size was 1.04 ± 0.3 mm and mean number of Table 2 Distribution of intracapsular effusions in the proximal and distal interphalangeal joints of each hand in the patients with finger osteoarthritis. Ray
Dominant hand Nondominant hand
PIP DIP PIP DIP
Total
2
3
4
5
11 14 10 15
15 23 15 19
15 15 20 8
16 13 11 8
PIP: proximal interphalangeal joints; DIP: distal interphalangeal joints.
57 65 56 50
S. Arrestier et al. / Joint Bone Spine 78 (2011) 65–69
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effusions per patient (counting both sides) was 2.05 ± 2.03. The PIP joint effusions were evenly distributed between the dominant and nondominant side, as well as among the four fingers studied on each side (Table 2). 4.1.2. Intracapsular effusions of the distal interphalangeal joints Of the 440 DIP joints, 115 (26%) showed effusions. Mean effusion size was 1.15 ± 0.5 mm and mean number of effusions per patient (both sides) was 2.09 ± 1.87. The DIP joint effusions were evenly distributed between the dominant and nondominant side, as well as among the four fingers studied on each side (Table 2). 4.1.3. Subtendinous effusions Overall subtendinous effusions were seen in 107 (24.2%) PIP joints and one DIP joint. On the dominant side, subtendinous effusions were seen in 60 PIP and zero DIP joints; corresponding figures on the nondominant side were 47 and one. The subtendinous effusions were evenly distributed between the dominant and nondominant side but preferentially affected the third PIP joint (21.3% on the dominant side and 19.5% on the nondominant side). 4.1.4. Synovitis None of the PIP or DIP joints in the patients with finger osteoarthritis showed evidence of synovitis. 4.1.5. Power Doppler imaging Joints with intracapsular or subtendinous effusions were examined using power Doppler imaging to look for hypervascularization. Of the 440 PIP joints, three showed grade 1 signals and one showed a grade 2 signal. Of the 440 DIP joints, 15 showed grade 1 signals and one showed a grade 3 signal; these signals were distributed evenly between the dominant and nondominant sides but preferentially affected the second DIP (n = 6) and third DIP (n = 8) joints. The power Doppler signals were typical for inflammation and did not suggest physiological vascularization (Fig. 1). 4.2. Comparison of ultrasound findings between patients and controls For intracapsular effusions of the PIP joints, no statistically significant differences were found between the patients and the controls (Fisher’s exact test, P > 0.05) (Table 3). In contrast, intracapsular effusions of the DIP joints were significantly more common in the patients than in the controls (P < 0.05) (Table 4). For subtendinous effusions in the PIP joints, no statistically significant differences were found between the patients and the controls (Fisher’s exact test, P > 0.12 for all PIPs, on the dominant and nondominant sides). A single subtendinous effusion was found in a DIP joint, which precluded a statistical evaluation of this feature. Similarly, the small number of Doppler signals in the patients and absence of Doppler signals in the controls precluded a meaningful statistical evaluation. However, it is interesting to note that hypervascularization, although rare, can occur in finger osteoarthritis and is then usually seen as a low-grade signal.
Fig. 1. a: ultrasonography abnormalities in finger osteoarthritis; b: palmar view showing an intracapsular effusion and an osteophyte, with no Doppler signal; c: palmar view showing an effusion and a grade 3 Doppler signal.
4.3. Correlations In the patients with finger osteoarthritis, we looked for correlations linking the ultrasonography findings to the clinical and radiographic manifestations, by computing the kappa coefficients. Clinical flares were not significantly correlated with presence of an intracapsular effusion by ultrasonography (Ä = 0.14) or a positive Doppler signal (Ä = 0.06). Neither were radiographic changes correlated with presence of an intracapsular effusion by ultrasonography (Ä = 0.03) or a positive Doppler signal (Ä = 0.0105). 5. Discussion Ultrasonography was recently investigated as a tool for evaluating osteoarthritis [4,5]. However, few studies have focused on ultrasonography findings in osteoarthritis of the hands. In 2007, 15 experts conducted a systematic literature review [11], which identified only two relevant studies [12,13]. The objective of the study was to develop a preliminary ultrasonographic scoring system for hand osteoarthritis. In each of seven patients, 15 joints of the dominant hand were examined (five metacarpophalangeal joints, five PIP joints, four DIP joints and the thumb metacarpophalangeal joint). Synovial hypertrophy and joint effusions were assessed using OMERACT criteria [10]. Power Doppler signals and osteophytes were also recorded. Intraobserver and interobserver
Table 3 Intracapsular effusions in the proximal and distal interphalangeal joints in the patients with finger osteoarthritis and in the healthy controls. PIP
Effusion (n/%) Effusion size in mm, mean ± SD Number of effusions/patient, mean ± SD Doppler signal (n/%)
DIP
Patients
Controls
Patients
Controls
113/25.7 1.04 ± 0.3 2.05 ± 2.03 4/3.5
77/21 0.83 ± 0.25 1.6 ± 1.7 0
115/26 1.15 ± 0.5 2.09 ± 1.87 16/13.9
11/2.1 0.72 ± 0.16 0 ± 0.6 0
PIP: proximal interphalangeal joints; DIP: distal interphalangeal joints.
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S. Arrestier et al. / Joint Bone Spine 78 (2011) 65–69
Table 4 Distribution of intracapsular effusions in the distal interphalangeal joints in patients with finger osteoarthritis and in healthy controls. DIP 2
Dominant hand Nondominant hand
DIP 3
DIP 4
DIP 5
OA
C
OA
C
OA
C
OA
C
14 P < 0.01 15 P < 0.01
0
23 P < 0.01 19 P < 0.01
2
15 P = 0.047 8 P = 0.106
5
13 P = 0.003 8 P = 0.007
1
0
1
2
0
DIP: distal interphalangeal joint; OA: patient with finger osteoarthritis; C: healthy control.
correlation coefficients were acceptable for these three features. These preliminary results suggest that ultrasonography may hold promise for evaluating osteoarthritis and provide a basis for developing an ultrasonography score [11]. More recently, a study of 1106 joints in 37 patients with hand osteoarthritis compared ultrasonography and standard radiography for evaluating the joint spaces and detecting osteophytes at the fingers [14]. Erosions were not studied. Compared to standard radiography, ultrasonography performed better for detecting osteophytes (Ä = 0.54) and metacarpophalangeal joint space narrowing [14]. We described nonstructural abnormalities (synovial hypertrophy, effusions, and Doppler signal) in patients with finger osteoarthritis. Osteophytes and erosions were not investigated. Erosions are difficult to detect by ultrasonography in fingers with osteoarthritis, both because they develop chiefly within bones and because they are often concealed by osteophytes. Furthermore, in everyday practice, the most common problem is the diagnosis of early osteoarthritis, often before the development of structural changes. We used a group of healthy controls to detect differences between normal and abnormal ultrasonography findings. We decided to use controls not older than 40 years of age to minimize the rate of undiagnosed asymptomatic osteoarthritis lesions in the control group. The absence of matching of the controls to the patients on age and sex may have introduced a bias, as the rates of synovial hypertrophy and joint effusions may vary with age and sex. However, a recent study of ultrasonography findings in patients with symptomatic finger osteoarthritis and in age- and sex-matched controls found significantly larger numbers of abnormalities in the patients [15]. The discrepancies between this study [15] and ours may be related to the exclusion from our study of structural changes (joint space narrowing and osteophytes) and of the metacarpophalangeal, carpometacarpal, and thumb PIP joints. However, the osteoarthritis changes predominantly affected the DIP joints. In our study, the number of effusions at the PIPs was not greater in the patients than in the controls, although the effusions were slightly larger (1.04 ± 0.3 mm versus 0.83 ± 0.25 mm). An ultrasonography study of patients with rheumatoid arthritis showed an increase in synovial thickness at the PIP joints compared to healthy controls (1.25 ± 0.87 mm versus 0.38 ± 0.34 mm), the optimal cutoff for distinguishing normal from abnormal PIP joints being 0.6 mm [16]. In our study, the only statistically significant difference between the patients and the controls was a higher rate of DIP joint effusions in the patients. Again, the size of these effusions seemed greater in the patients. A study in 15 patients with PsA and five with RA, as well as in five healthy controls, compared ultrasonography to standard radiography and magnetic resonance imaging [17]. Ultrasonography detected a larger number of DIP joint abnormalities in the PsA patients than in the RA patients or controls, but these lesions consisted chiefly in bone proliferation rather than in synovial hypertrophy, which was seen in 22% of DIP joints in the PsA group compared to 23% in the RA group and 3% in
the control group. Power Doppler imaging was not performed [17]. A large number of PIP joints in our study exhibited subtendinous effusions at the palmar side, with no difference between patients and controls. As pointed out in our previous study [7], the meaning of these effusions is unclear. Power Doppler imaging indicated hypervascularization of four PIP and 16 DIP joints in our patients and none of our controls. The small number of joints with hypervascularization precluded a statistical evaluation. Thus, further investigation of this feature is needed. In a group of patients with erosive finger osteoarthritis, power Doppler imaging showed a considerably higher rate of hypervascularization (22.4% of joints) [18]. However, another study of patients with finger osteoarthritis found no correlation between presence of a clinical flare and presence of an intracapsular effusion with or without a power Doppler signal [15]. Our study indicates that the main differences in nonstructural lesions between healthy individuals and patients with finger osteoarthritis are found at the DIP joints. Effusions in the PIP joints do not seem to reliably indicate disease. To better delineate the ultrasonography features of the PIP joints, a comparison with RA patients would be of interest. For the DIP joints, comparing the ultrasonography findings to those in patients with PsA may prove useful. Finally, in both the patients and the healthy controls, and at both the PIP joints and the DIP joints, the abnormalities were usually seen at the palmar aspect of the fingers. In patients with pain and swelling of the PIP and DIP joints, ultrasonography delineates the lesions, providing objective data for distinguishing between inflammatory joint disease and osteoarthritis. Available studies suggest a key diagnostic role for ultrasonography, most notably in doubtful cases.
Conflict of interest statement The authors have no conflict of interest to declare.
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