Detection of Enthesitis in Children with Enthesitisrelated Arthritis

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Detection of Enthesitis in Children with Enthesitisrelated Arthritis ARTHRITIS & RHEUMATOLOGY Vol. 66, No. 1, January 2014, pp 218–227 DOI 10.1002/art.38197 © 2014, American College of Rheumatology Detection of Enthesitis in Children With Enthesitis-Related Arthritis Dolorimetry Compared to Ultrasonography Pamela F. Weiss,1 Nancy A. Chauvin,1 Andrew J. Klink,1 Russell Localio,2 Chris Feudtner,1 Diego Jaramillo,1 Robert A. Colbert,3 David D. Sherry,1 and Ron Keren1 Objective. To evaluate the distribution of enthesi- interval [95% CI] 0.63–0.93), and the interrater reliabil- tis and the accuracy of physical examination with a ity was 0.81 (95% CI 0.67–0.95). Tenderness as detected dolorimeter for the detection of enthesitis in children, by standardized dolorimeter examination had poor pos- using ultrasound (US) assessment as the reference itive predictive value for US-confirmed enthesitis. In standard. comparison to controls, patients with ERA reported Methods. We performed a prospective cross- more pain and had lower pain thresholds at every site, sectional study of 30 patients with enthesitis-related including control sites (P < 0.001 for all comparisons). arthritis (ERA) and 30 control subjects. The following The interrater reliability of dolorimeter examination CI %95] 0.49 ؍ tendon insertion sites were assessed by standardized for detection of enthesitis was low (␬ physical examination with a dolorimeter and US: com- 0.33–0.65]). mon extensor on the lateral humeral epicondyle, com- Conclusion. Compared to US, standardized dolo- mon flexor on the medial humeral epicondyle, quadri- rimeter examination for the detection of enthesitis in ceps at the superior patella, patellar ligament at the children has poor accuracy and reliability. The de- inferior patella, Achilles, and plantar fascia at the creased pain threshold of ERA patients likely contrib- calcaneus. uted to the limited accuracy of the physical examination Results. Abnormal findings on US were detected findings. Further research regarding the utility of US most commonly at the insertion of the quadriceps (30% for identifying enthesitis at diagnosis of juvenile idio- [18 of 60 sites]), common extensor (12% [7 of 60]), and pathic arthritis, accurately predicting disease progres- Achilles (10% [6 of 60]) tendons. The intrarater reli- sion, and guiding therapeutic decisions is warranted. ability of US (kappa statistic) was 0.78 (95% confidence Enthesitis refers to inflammation at the attach- Dr. Weiss’s work was supported by the NIH (National ments of the ligaments, tendons, and joint capsules to Institute of Arthritis and Musculoskeletal and Skin Diseases grant 1-K23-AR059749-01A1); she is also recipient of a Rheumatology the bone. It is a distinct clinical hallmark of the spondy- Research Foundation Bridge Funding award. Dr. Colbert’s work was loarthropathies (SpA) in both children and adults. In supported by the NIH (National Institute of Arthritis and Musculo- children, enthesitis is usually diagnosed by clinical find- skeletal and Skin Diseases Intramural Research Program grant Z01- AR-041184). ings, including localized pain, tenderness, and swelling. 1Pamela F. Weiss, MD, MSCE, Nancy A. Chauvin, MD, These features, however, are nonspecific and can also Andrew J. Klink, MPH, Chris Feudtner, MD, PhD, MPH, Diego be found in normal children (1) and in patients with Jaramillo, MD, David D. Sherry, MD, Ron Keren, MD, MPH: Children’s Hospital of Philadelphia, Philadelphia, Pennsylvania; overuse injuries, apophysitis, and fibromyalgia. In adult 2Russell Localio, MPH, MS, PhD: University of Pennsylvania, SpA, magnetic resonance imaging (MRI) and ultra- Perelman School of Medicine, Philadelphia, Pennsylvania; 3Robert A. sound (US) with power Doppler are used to distinguish Colbert, MD, PhD: National Institute of Arthritis and Musculoskeletal and Skin Diseases, NIH, Bethesda, Maryland. inflammatory enthesitis from these other conditions Address correspondence to Pamela F. Weiss, MD, MSCE, (2–4). In studies that used these imaging modalities as Children’s Hospital of Philadelphia, 3535 Market Street, Room 1526, the reference standard in the evaluation of adult SpA, Philadelphia, PA 19104. E-mail: [email protected]. Submitted for publication June 20, 2013; accepted in revised physical examination had poor sensitivity for detecting form September 10, 2013. inflammatory enthesitis (2), and US was a useful tool 218 ULTRASOUND VERSUS PHYSICAL EXAMINATION FOR PEDIATRIC ENTHESITIS 219 Figure 1. Ultrasound examination of the common extensor tendon insertion at the lateral elbow using a Philips IU22 machine with a high-frequency linear-array 12-MHz transducer. Power Doppler imaging was performed in long and transverse planes. A, Images were acquired with the elbow in mild flexion and the forearm pronated. B, An image from the gray-scale evaluation shows the thickness of the tendon, as delineated by the arrowheads.LEϭ lateral epicondyle; R ϭ radial head. C, An image from the Doppler evaluation shows moderate vascularization. Red regions are increased power Doppler signals, which indicate increased vascularity. for following the response of enthesitis to treatment (5). during the examination and performed US as the refer- In those studies, the sensitivity of the physical examina- ence standard test at the same visit. tion findings was low, ranging from 0.16 to 0.22, and the specificity was moderate, ranging from 0.80 to 0.87 (2,6). PATIENTS AND METHODS The sensitivity, specificity, positive predictive Human subjects protections. The protocol for the value (PPV), and negative predictive value (NPV) of conduct of this study was approved by the Committee for the clinical examination for the detection of enthesitis have Protection of Human Subjects at the Children’s Hospital of been sparsely studied in juvenile idiopathic arthritis Philadelphia (CHOP). (JIA) (7,8). The accurate diagnosis of enthesitis is Study subjects. The study subjects were a convenience important because its presence has implications with sample drawn without regard to disease duration, severity, or current activity or therapy from a source population of chil- regard to the classification of JIA, which in turn, influ- dren with a diagnosis of ERA who were 5–18 years of age and ences treatment decisions and monitoring for extra- had been evaluated at the CHOP Rheumatology Clinic be- articular manifestations of the disease. Currently, physi- tween March 2011 and February 2013. All patients met the cians vary with regard to which entheses they evaluate, ILAR criteria for ERA (9), according to the treating physician. the amount of pressure they apply, and what criteria they The presence of at least 1 tender enthesis on physical exami- nation performed at the screening visit was required in order use to diagnose positive findings (e.g., verbal indication for an ERA patient to be eligible for study. Exclusion criteria of pain or withdrawal upon pain). The International were contraindications for performing US, including local League of Associations for Rheumatology (ILAR) cri- malignancy, metal implants below the area of examination, teria for JIA classifies many children with SpA as having localized tissue or bone infections, or vascular abnormalities. enthesitis-related arthritis (ERA) (9) based solely on the Healthy control subjects were recruited from a local primary care practice and were age- and sex-matched to the patients. presence of enthesitis. Clinical data. We collected self-reported information In the present study, we sought to evaluate the on sex, age, race, ethnicity, and family history of rheumatic distribution of enthesitis and the accuracy of physical disease. We abstracted information about medications (past examination for the detection of enthesitis in children. and current), disease duration, HLA–B27 status, and antinu- We examined 6 bilateral entheses in children with ERA, clear antibody (ANA) status from the electronic health record. Health status measures. The patients (if at least 13 the category of JIA with the highest prevalence of years of age) or their parents or legal guardians completed the enthesitis, as well as in healthy controls. We used a following 5 health status questionnaires: the Pediatric Rheu- dolorimeter to objectively measure the pressure applied matology Quality of Life (PRQL) (10), the Childhood Health 220 WEISS ET AL Table 1. Demographic and clinical features of the study subjects* ERA patients Control subjects (n ϭ 30) (n ϭ 30) Age at visit, median (IQR) years 13 (11–15) 12 (7–15) Disease duration, median (IQR) years 0.6 (0.1–2.6) – No. (%) male 18 (60) 16 (52) Criteria for ERA diagnosis, no. (%) Enthesitis 30 (100) – Arthritis 29 (97) – Inflammatory back pain 14 (47) – Acute symptomatic uveitis 2 (7) – Onset of arthritis in a male Ն6 years of age† 17 (94) – HLA–B27 positive 9 (30) – Family history of AS, ERA, IBD with associated sacroiliitis, 7 (23) – acute uveitis, or ReA in a first-degree relative No. of joints with active arthritis, median (IQR)‡ 2 (1–2) 0 (0) Erythrocyte sedimentation rate, median (IQR) mm/hour‡ 0 (0–12) – C-reactive protein, median (IQR) mg/dl 0 (0–0.5) – PRQL score, median (IQR) 6.5 (3–10) 0 (0–1) Patient’s/parent’s assessment of pain over the previous week, 4 (2–7) 0 (0–0) by VAS, median (IQR) score C-HAQ score, median (IQR) 0.31 (0.13–0.88) 0 (0–0) BASFI, median (IQR) 1.6 (0.7–4.9) 0 (0–0) BASDAI, median (IQR) 3.8 (2.6–6.4) 0 (0–0) Current medications, no. (%) Daily NSAIDs 19 (63) – DMARDs 7 (23) – Anti-TNF agents Etanercept 8 (27) – Infliximab 2 (7) – Adalimumab 1 (3) – * ERA ϭ enthesitis-related arthritis; IQR ϭ interquartile range; AS ϭ ankylosing spondylitis; IBD ϭ inflammatory bowel disease; ReA ϭ reactive arthritis; PRQL ϭ Pediatric Rheumatology Quality of Life; VAS ϭ visual analog scale; C-HAQ ϭ Childhood Health Assessment Questionnaire; BASFI ϭ Bath Ankylosing Spondylitis Functional Index; BASDAI ϭ Bath Ankylosing Spondylitis Disease Activity Index; NSAIDs ϭ nonsteroidal antiinflammatory drugs; DMARDs ϭ disease-modifying antirheumatic drugs; anti-TNF ϭ anti– tumor necrosis factor. † Results apply only to the 18 male patients.
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