DIAGNOSTIC ASSOCIATIONS WITH HYPERMOBUJTY IN RHEUMATOLOGY PATIENTS
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1 British Journal of Rheumatology 1995;34: DIAGNOSTIC ASSOCIATIONS WITH HYPERMOBUJTY IN RHEUMATOLOGY PATIENTS N. HUDSON, M. R. STARR, J. M. ESDAILE and M.-A. FTTZCHARLES Rheumatic Disease Unit, McGill University, Montreal, Quebec, Canada SUMMARY Although we have considerable Icnowledge of the demographic characteristics of hypermobile individuals in population studies, we have little understanding of the implications of hypermobility. In this rheumatology clinic-based study we assessed the prevalence, diagnostic associations and clinical features of hypermobility in consecutive newly referred patients. Hypermobility was identified in 50 of 378 patients (13.2%). The most common clinical diagnosis in the hypennobile patients, compared with controls (those without hypermobility), was soft tissue rheumatism observed in 67% vs 25% (P < 0.001). Fibromyalgia syndrome was the most common specific rheumatological diagnosis in 30% vs 8% (P < 0.001) and inflammatory arthritis the least common diagnosis in 4% vs 32% (P < 0.001) of hypermobile versus non-hypermobile patients, respectively. Hypermobile patients complained of previous pain, including widespread or multiple localized sites of pain and spinal pain. Although clinic-based studies may not accurately reflect disease patterns as seen in the population, these results suggest an association between hypermobility and soft tissue rheumatic complaints and should be useful to the clinical rheumatologist. KEY WORDS: Hypermobility, Rheumatology practice, Soft tissue rheumatism, Fibromyalgia syndrome. THERE is increasing knowledge of the range of articular motion in various racial, population and selected occupational groups, but little attention has been given to the clinical implications of an individual having lax ligaments. The consequences of hypermobility are not clearly understood and the frequency of musculoskeletal complaints in persons who are hypermobile is unknown. A recent study of musicians [1] indicated that increased joint mobility may be an advantage when performing the repetitive activity of playing an instrument, but a disadvantage when a supporting area, such as the knee or spine, is involved and associated with prolonged immobility. Hypermobility may be defined as increased mobility of small and large joints beyond the range of motion considered normal. The hypermobility syndrome is defined as generalized joint laxity with associated musculoskeletal complaints in the absence of any other demonstrable systemic rheumatic disease [2]. It has been well demonstrated that mobility varies according to sex [3-10], age [3-5, 7, 8, 11, 12] and ethnic background [3, 10, 12]. Hypermobile joints are more prevalent in younger females of black or Asian origin. Joints tend to stiffen and lose mobility with ageing. The overall frequency of hypermobility is difficult to determine as mild degrees of, or localized hypermobility may occur in asymptomatic individuals. Studies to date indicate that 5-15% of the Caucasian adult population [1,4,6,8], as well as rheumatology patients [6], would be classified as hypermobile. Only one recent report has focused on specific rheumatological complaints encountered in adult patients with hypermobile joints [6]. Although there is Submitted 24 March 1995; revised version accepted 24 July Correspondence to: M.-A. Fitzcharles, Royal Victoria Hospital, 687 Pine Avenue West, Montreal, Quebec, H3A 1A1, Canada. an impression that hypermobility and soft tissue complaints may be related, this has never been specifically addressed in the context of rheumatology clinic patients. The present study was designed to assess the prevalence of hypermobility in a rheumatology referral population and to determine whether there might be any relationship between musculoskeletal complaints and hypermobility. Particular attention was paid to a history of previous episodes of musculoskeletal pain as well as to the current musculoskeletal problem, including presence of soft tissue rheumatism, spinal or peripheral joint pain. Physical activity as well as a history of prolonged immobility, both occupational and leisure, was recorded. PATIENTS AND METHODS A total of 378 consecutive newly referred rheumatology adult patients of 16 yr and over were prospectively screened for generalized hypermobility according to the Beighton [3] modification of the Carter and Wilkinson criteria [13]. Patients were given a score of 0-9, one point being allocated for the ability to perform each of the following tests: (1) passive dorsiflexion of the little finger beyond 90 ; (2) passive apposition of the thumb to the flexor aspects of the forearm; (3) hyperextension of the elbow beyond 10 ; (4) hyperextension of the knee beyond 10 ; and (5) forward flexion of the trunk, with the knees straight, so that the palms of the hands rested easily on the floor. Patients were considered hypermobile if they scored 4 or greater out of 9. Demographic data included age, sex and primary clinical diagnosis. The major diagnostic category groups were: inflammatory arthritis (including seropositive and seronegative rheumatoid arthritis, psoriatic" arthritis, Reiter's syndrome, crystal arthropathy and inflammatory spondyloarthropathy); osteoarthritis; axial pain (including neck and low-back pain); and soft tissue rheumatism (including bursitis, tendonitis and British Society for Rheumatology
2 1158 BRITISH JOURNAL OF RHEUMATOLOGY VOL. 34 NO. 12 fibromyalgia syndrome). Of the 378 patients, 50 fulfilled criteria for hypermobility and were invited to attend for a second interview, at which time a history and physical examination was performed according to a standard physician-administered protocol, approved by the Ethics Committee of the Royal Victoria Hospital. Patients signed an informed consent form. The questionnaire included information regarding a previous history and localization of musculoskeletal symptoms, including pain, soft tissue rheumatism, either bursitis or tendinitis, and spinal symptoms. A history of physical activity was recorded, including sporting activity, repetitive activity or prolonged immobility, both at leisure and at work. Patients were examined according to the mobility scoring system of Beighton [3] and Bulbena [9] (Fig. 1). In addition, patients were examined for the presence of tender points according to American College of Rheumatology (ACR) criteria for fibromyalgia syndrome [14], clinical evidence of osteoarthritis, present sites of musculoskeletal pain and signs of thoracic outlet syndrome [15]. Symptoms suggestive of thoracic outlet syndrome were defined as an aching pain and/or paraesthesiae extending from the lateral neck across UPPER ARM the shoulder and down the forearm and aggravated by positional changes, particularly raising the arms above shoulder level. Reproduction of these symptoms by abduction and lateral rotation of the arm at the shoulder with concomitant loss of the radial pulse at the wrist was taken as a positive test for thoracic outlet compression. Auscultation for a bruit over the subclavian artery during this manoeuvre was performed. A history of widespread pain according to the ACR criteria for fibromyalgia syndrome was noted [14]. Statistical analysis for categorical variables was performed using the Chi-square test, and when small numbers were present (any cell <. 5) Fisher's exact test was used. Continuous variables were contrasted with Student's /-test. RESULTS Hypermobility was identified in 50 of the 378 patients screened, giving a frequency of 13.2% in all newly referred rheumatology patients. Female patients numbered 47 (94%) in the hypermobile group and 282 (73%) in the control group. The average age 1 THUMB: Passive apposition of the thumb to the flexor aspect of the forearm at < 21 mm. 2 METACARPOPHALANGEAL: With the palm of the hand resting on the table, the passive dorsiflexion of the fifth finger is Z ELBOW HYPEREXTENSION: The passive hyperextension of the elbow is S EXTERNAL SHOULDER ROTATION: With the upperarm touching the body and with the elbow flexed at 90, the forearm is taken in external rotation up to > 85 of the sagittal plane (shoulder to shoulder line). LOWER EXTREMITIES. SUPINE POSITION 5 HIP ABDUCTION: The passive hip abduction can be taken to an angle of ROTULAR HYPERMOBILITY: Holding with one hand the proximal end of the tibia, the rotula can be moved well to the sides with the other hand. FIG. 1. Hospital del Mar (Barcelona) criteria for the clinical assessment of joint hypennobility (derived from [9D- 7 ANKLE AND FEET HYPERMOBILITY: An excess range of passive dorsiflexion of the ankle and eversion of the foot can be produced. 8 METATARSOPHALANGEAL: Dorsal flexion of the toe of the foot over the diaphysis of the first metatarsal is LOWER EXTREMITIES. PRONE POSITION 9 KNEE HYPERFLEXION: Knee flexion allows the heel to make contact with the buttock. 10 ECCHYMOSES: Appearance of ecchymoses after hardly noticed, minimal traumatism. HYPERMOBIIJTY SCORING SYSTEM: Using 1 point per item (overall range 0 to 10); males classified as hypermobile by score i 4 and females classified as hypermobile by score S.
3 HUDSON ET AL.: HYPERMOBILITY IN RHEUMATOLOGY PRACTICE 1159 TABLE I Primary diagnostic categories of 374 newly referred rheumatology patients Fibromyalgia Bursi Us/tendinitis Axial pain Osteoarthritis Inflammatory Miscellaneous Hypermobility syndrome Hypermobile (n=46) n (%) 14 (30) 12 (26) 7(15) 3(7) 2(4) 3(7) 5(11) Controls (n = 328) n (V.) 26(8) 57 (17) 48(15) 62 (19) 105 (32) 30(9) 0(0) P value* < < <0.00I Chi-square unless any cell < 5, in which case Fisher's exact test (two-tailed) was used. of hypermobile patients was 45.5 yr (range yr) and of control patients was 53.3 yr (range yr). Four of the 50 hypermobile patients did not consent to further clinical evaluation. Of the 46 hypermobile patients meeting the Beighton criteria, 42 (91%) met the Bulbena criteria [9] for diffuse hypermobility. Demographic and clinical data were available on 328 non-hypermobile patients who served as the control group. Table I shows the primary diagnostic categories of patients studied. The most frequent diagnosis in the hypermobile patients was fibromyalgia syndrome in 14 (30%). Soft tissue rheumatism, including tendinitis, bursitis or fasciitis, occurred in 12 (26%) hypermobile patients compared with 57 (17%) controls. Spinal complaints were identified with equal frequency in the two groups. However, the hypermobile group, compared with the control group, demonstrated less osteoarthritis at 7% versus 19%, and significantly less inflammatory arthropathy at 4% versus 32%. In the hypermobile group one patient was diagnosed with rheumatoid arthritis and one with psoriatic arthritis. Of the 46 hypermobile patients a primary diagnosis of hypermobility syndrome was made in five (11%) female patients. Overall, 31 (67%) hypermobile patients had symptoms attributable to soft tissue complaints, including fibromyalgia syndrome, bursitis, tendinitis or hypermobility syndrome. Other diagnoses, including entrapment neuropathies, reflex sympathetic dystrophy syndrome, vasculitis and myopathies, were identified equally in the two groups. Table II shows the pattern of previous and current musculoskeletal symptoms experienced by the 46 hypermobile patients studied. Of note, widespread musculoskeletal pain had occurred at some time in 20 (44%) of the hypermobile patients. Multiple distinct sites of pain had occurred in a further 20 (44%) and only six (13%) of the hypermobile group had experienced musculoskeletal symptoms at only one localized site. A history of spinal complaints, including neck pain in 17 (37%) and mechanical mid-thoracic and low-back pain in 37 (80%), was also prominent in these patients. No particular body zone, either spinal, upper limb or lower limb, was predominantly affected in this hypermobile population. Symptoms suggestive of thoracic outlet syndrome were reported commonly in this group of patients (54%) and could be diagnosed in 13 (28%), as defined by absence of pulse and reproduction of symptoms when abducting and externally rotating the arm at the shoulder. Specific physical activities reported by hypermobile patients included a history of repetitive activity in 19 patients, prolonged immobility in 13 patients and participation in leisure sports in 16 patients. These patterns of physical activity did not discriminate between the sites of pain, either upper or lower limb, spinal or widespread pain or presence of fibromyalgia syndrome in patients with hypermobile joints. DISCUSSION In contrast to various opinions, only scant information is available about the risks associated with hypermobility. March and Silman [16] have recently questioned whether there might be a case for screening individuals for hypermobility in order to prevent musculoskeletal problems in the future. This clearly would be valid if there is an association between hypermobility and musculoskeletal complaints, particularly in the work-related environment. Our data indicate that ligamentous laxity is a common finding in patients referred to rheumatologists for musculoskeletal symptoms. The most frequent clinical diagnosis for hypermobile patients was soft tissue rheumatism, including tendinitis, bursitis andfibromyalgiasyndrome. This is the first study to suggest that there might be an association between hypermobile joints and rheumatic complaints in patients referred for rheumatological opinion. Only two of the 46 hypermobile patients in the present study were diagnosed as having an inflammatory arthropathy. This is contrary to the findings of Bridges el al. [6], who reported 25% hypermobile patients with a diagnosis of systemic lupus erythematosus or rheumatoid arthritis. Our study may have underestimated previous hypermobility in patients with inflammatory or degenerative arthropathy and older patients. The importance of previous hypermobility in patients with an inflammatory arthritis is not known. However, a number of TABLE II Musculoskeletal complaints experienced by 46 hypermobile patients Pain Widespread Multiple localized sites Single localized site Spinal neck Spinal thoracic/low back Upper limbs Lower limbs Thoracic outlet syndrome Symptoms Positive test manoeuvre Tendinitis (previous and present) Inflammatory arthritis Number Percentage Aching pain and/or paraesthesiae across the shoulder and down the forearm following abduction and lateral rotation of the arm at the shouldet, with concomitant loss of radial pulse at the wrist
4 1160 BRITISH JOURNAL OF RHEUMATOLOGY VOL. 34 NO. 12 studies have suggested that premature osteoarthritis may be associated with, and possibly the consequence of, hypermobility [2, 6, 11, 17]. Osteoarthritis was not commonly recognized in the present cross-sectional study but was the most common diagnosis observed in 60% of hypermobile patients reported by Bridges et al. [6]. A further five (11%) in the present study had musculoskeletal symptoms, arthralgias and myalgias without any other specific clinical diagnosis, and would be classified as presenting with hypermobility syndrome. Overall, 31 (67%) hypermobile rheumatology clime patients had symptoms attributable to soft tissue disorders or hypermobility syndrome. Since patients in this study were recruited through referral to a rheumatology clinic, we are unable to make any comment upon the frequency of hypermobility in the general population. Clinic-based studies are limited in that they may not truly reflect disease status in populations, but may help towards our overall understanding of disease processes. The recorded frequency of hypermobility is 5-13% in childhood [18, 19], 4-5% in the general population [4] and up to 15% in rheumatology clinics [6]. Hypermobility was identified in 13% of all newly referred rheumatology patients in the present study. In accord with other series we have identified hypermobility more commonly in younger females. The 9-point Beighton scoring system is an all-ornone system and does not take into account degree of mobility, localized hypermobility or change in mobility with ageing [3]. The Bulbena scoring system includes in addition assessments of shoulder, patellar and ankle mobility, which are common sites of musculoskeletal pain, and may represent more meaningful measurements in the practical management of patients [9]. We are unable to make any statement concerning localized hypermobility which might be associated with the development of musculoskeletal pain in specific areas. This may be an important factor in some occupational or sporting related musculoskeletal symptoms and warrants further investigation. Little attention has been paid to the causation of musculoskeletal symptoms in hypermobile individuals. Some previous studies have suggested that increased ligamentous laxity may be associated with soft tissue rheumatism and ligamentous injury [2,6,20,21]. It would seem plausible that excessive ligamentous laxity might predispose a patient to episodes of tendon strain manifest as recurrent episodes of tendonitis. It has been well documented that hypermobile children have articular symptoms [19] as well as an increased frequency of fibromyalgia syndrome [19]. It is not known whether there is any association between hypermobility in the adult and symptoms. of fibromyalgia syndrome. Fibromyalgia was the primary rheumatological working diagnosis in 30% of the present hypermobile group studied and was the most common specific rheumatological diagnosis in this group. The hypermobile fibromyalgia syndrome patients did not differ from other hypermobile patients in their physical activity, including prolonged immobility or repetitive activity, or their participation in sporting activities. " Complaints of previous widespread musculoskeletal pain as well as multiple localized sites of pain were a common symptom reported by hypermobile patients, irrespective of their specific current rheumatological diagnosis. A symptom of widespread pain may be indicative of fibromyalgia syndrome or a variant thereof, and strict adherence to ACR criteria for fibromyalgia may be too restrictive. Patients with previous or intermittent widespread pain and hypermobility may have a variant of or intermittent fibromyalgia syndrome. Of note, only 13% of hypermobile patients gave a history of a specific single localized site of pain. In addition, symptoms suggestive of thoracic outlet obstruction, characterized by aching of the arms on elevation as well as the development of paraesthesiae, were reported by over half of the hypermobile patients, with a positive test manoeuvre occurring in 28%. Ligamentous laxity may be an important factor in the anatomical changes resulting in a pressure phenomenon of the thoracic outlet syndrome. Recognition of hypermobility may be useful for the clinical rheumatologist and be relevant in assessing patients with recurrent soft tissue rheumatism and sports and work-related injuries. Localized hypermobility may be as important as generalized hypermobility, particularly in the context of physical activities requiring either excessive localized repetitive activity or prolonged periods of immobility [1]. Future studies are needed to determine whether activity patterns, both at work and at leisure, have any influence upon musculoskeletal symptom development in hypermobile individuals. A diagnosis of hypermobility may be important in order to identify aggravating factors and introduce preventative measures. An increased appreciation of hypermobility in patients might prevent unnecessary investigation and allow for physical treatment measures directed towards improving muscle tone and prevention of recurrent soft tissue microtrauma. REFERENCES 1. Larsson L-G, Baum J, Mudholkar GS, Kollia GD. Benefits and disadvantages of joint hypermobility among musicians. N Engl J Med 1993^29: Kirk JA, Ansell BM, Bywaters EGL. The hypermobility syndrome. Musculoskeletal complaints associated with generalized joint hypermobility. Ann Rheum Dis : Beighton P, Solomon L, Soskolne CL. Articular mobility in an African population. Ann Rheum Dis 1973^2: Jessee EF, Owen DS, Sagar KB. The benign hypermobile joint syndrome. Arthritis Rheum 1980;23:105>6. 5. Silman AJ, Day SJ, Haskard DO. Factors associated with joint mobility in an adolescent population. Ann Rheum Dis 1987;46: Bridges AJ, Smith E, Reid J. Joint hypermobility in adults referred to rheumatology clinics. Ann Rheum Dis 1992^1: Larsson L-G, Baum J, Mudholkar GS. Hypermobility:
5 HUDSON ET AL.: HYPERMOBILITY IN RHEUMATOLOGY PRACTICE 1161 features and differential incidence between the sexes. Arthritis Rheum 1987^30: Larsson L-G, Baum J, Mudholkar GS, Srivastava DK. Hypermobility: prevalence and features in a Swedish population. Br J Rheumatol 1993;32: Bulbena A, Duro JC, Porta M, Faus S, Vallescar R, Martin-Santos R. Clinical assessment of hypermobility of joints: assembling criteria. / Rheumatol 1992;19: Al-Rawi ZS, Al-Aszawi AJ, Al-Chalabi T. Joint mobility among university students in Iraq. Br J Rheumatol 1985:24: Bird HA, Tribe CR, Bacon PA. Joint hypermobility leading to osteoarthritis and chondrocalcinosis. Arm Rheum Dis 1978:37: Wordsworth P, Ogilvie D, Smith R, Sykes B. Joint mobility with particular reference to racial variation and inherited connective tissue disorders. Br J Rheumatol 1987:26: Carter C, Wilkinson J. Persistent joint laxity and congenital dislocation of the hip. / Bone Joint Swg 1964;46: Wolfe F, Smythe HA, Yunus MB et al. The American College of Rheumatology 1990 criteria for the classification of fibromyalgia: report of the multicenter criteria committee. Arthritis Rheum 1990:33: Leffert RD. Neurological problems. In: The shoulder. Rockwood CA Jr, Matsen FA III, eds. Vol. II. Philadelphia: WB Saunders, 1990: March L, Silman A. Joint hyperlaxity: is there a case for screening? Br J Rheumatol 1993:32: Scott D, Bird H, Wright V. Joint laxity leading to osteoarthritis. Rheumatol Rehabil 1979; 18: Biro F, Gewanter HL, Baum J. The hypermobility syndrome. Pediatrics 1983;72: Gedalia A, Press J, Klein M, Buskila D. Joint hypermobility andfibromyalgiain schoolchildren. Ann Rheum Dis 1993:52: Grahame R. The hypermobility syndrome. Ann Rheum Dis 1990:49: Nicholas JA. Injuries to knee ligaments. Relationship to looseness and tightness in football players. / Am Med Assoc 1970:212:
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