Idiopathic Destructive Arthritis of the Shoulder

Idiopathic Destructive Arthritis of the Shoulder

By G.V. Campion, F. McCrae, W. Alwan, I. Watt, J. Bradfield, and P.A. Dieppe

D ESTRUCTIVE ARTHRITIS of the shoulder joint is an uncommon condition.

It has been described in association with a variety of arthropathies, and as an idiopathic phenomenon. A literature search shows that it has been reported under a variety of names by several investigators. Comparisons of the various series of patients has not been attempted, and patients with and without an apparent cause have not been contrasted. As a result of recent interest in this disorder and its pathogenesis, a review of published data is timely. In this report, we dis- cuss several previous series and briefly describe a group of 50 patients with the condition. The literature review and our series of patients indi- cate that a similar clinical picture can result from a variety of starting points, and that similar pathogenic mechanisms may be involved.

HISTORICAL REVIEW

Writing in 1967 in L’actualitt rheumatologi- que,’ de Sbze reviewed recent reports of primary shoulder diseases in the elderly under the title “l’epaule Senile Htmorrhagique” (“Hemor- rhagic Shoulder of the Elderly”) and added novel observations of his own, de Seze quoted reports dating from 1958 by Galmiche and Deshayes,2 and included those by Burman et aL3 Banna and Humme Kendall: Shepard,’ and Snook,6 which considered the problem of spontaneous hemar- throsis in the elderly, involving some 30 observed cases affecting the sexes equally. Reports mainly concerned patients over 80 years old and only three were ~60. In de Seze ‘s view, the hemar-

From the Department of Medicine, University of Bristol, Bristol Royal Infirmary, England.

G.V. Campion, MB, BS, MRCP: Lecturer in Rheumatolo- gy; F. McCrae, MB, ChB, MRCP: Registrar; W. Alwan,

MD; Pathologist; I. Watt, MRCP, FRCR: Consultant Radi- ologist; J. Bradfield, BM, BCh, MRCP, PhD: Professor of Pathology; P.A. Dieppe, MD, BSc, FRCP: ARC Professor of Rheumatology.

Address reprint requests to P.A. Dieppe, BSc. MD. FRCP, Consultant Senior Lecturer in Rheumatology, University of Bristol, Department of Medicine. Bristol Royal Infirmary, Bristol BS2 8HW. England.

0 1988 by Grune & Stratton, Inc. 0049-0172/88/l 704-0013$5.00/O

throsis took two forms. The first was character- ized by a rapid loss of passive movement and no obvious preceding trauma, followed by extensive bruising, with blood-stained fluid obtained on joint aspiration. This type resolved over several days and was associated radiographically with minor degenerative changes of the glenohumeral joint and erosions of the greater tuberosity. The second form was more chronic, but could have an abrupt onset. However, it took longer to resolve, was associated with a larger effusion, and led to moderate residual impairment of function. Radiographs showed marked rotator cuff changes.

The novel aspect of this report was the description of three shoulders demonstrating what de Seze called “les caries seniles htmorrhagique de l’epaule,” or senile hemorrhagic decay of the shoulder. This condition combined rupture of the rotator cuff with major osteolysis to such a degree “that the initial impression was of a major destructive process such as tuberculosis or even a malignant tumor of the shoulder.” Several features of his patients militated against these diagnosis: the otherwise good general health, normal sedimentation rate, moderate pain and loss of function, and length of history. Surgical inter- vention in one confirmed a hemorrhagic effusion and large tear of the rotator cuff with no evidence of tumor or tuberculosis. Histological examination showed nonspecific inflammation only, with no evidence of villonodular synovitis.

We have dwelt at some length on de Seze’s report, as we consider it contains the essence of what subsequently has been described as Mil- waukee shoulder,’ cuff tear arthropathy,’ l’arthropathie destructrice rapide de l’epaule (ADRE), and apatite-associated destructive arthropathy (ADA).”

Apart from a single case report by Bauduin and Famaey in 1969,” l’tpaule senile htmorrhagique did not figure again in the literature until 1977, when in a study of nine cases, Lambo- ley et alI2 confirmed the age distribution of patients affected and noted that although trauma was attributed as a cause by most patients, it was often minor or temporarily remote. Eight of the nine cases presented were female. Clinically, the

232 Seminars in Arthritis and Rheumatism, Vol 17, No 4 (May), 1988: pp 232-245

DESTRUCTIVE ARTHRITIS OF THE SHOULDER 233

condition presented with a painful, poorly func- tioning shoulder with effusion and ecchymosis. Normal laboratory tests contrasted with the dra- matic radiological changes. Pain was of variable

onset, sometimes acute and self-limiting, or more frequently progressive with moderate, intermit- tent, or continuous pain. Nocturnal exacerbation of pain was reported sometimes. Swelling was found in 80%, and 50% had bruising, which was anterior or anterolateral and occasionally extensive, extending down the arm to the elbow. The course was that of rapid resolution of swelling and bruising within seven days, but with persis- tence of moderate functional disability for several weeks to months. Thirty percent relapsed within one week to one year. Aspiration of the shoulder showed sterile blood or a blood-stained

effusion. Plain x-rays demonstrated “degenerative changes” affecting the glenohumeral joint and the rotator cuff insertions, but others were

marked by destructive changes, including osteolytic lesions of the greater tuberosity, humeral head, acromion, and sometimes clavicle and glenoid fossa. In four patients, there was amputa- tion of the superior-lateral aspect of the humeral head. Chondrocalcinosis was noted in one case, which also affected the knees. Diffuse osteoporosis was also noted in two cases involving the humeral head and the acromion.

Lamboley noted that two of his patients had osteoarthritis (OA) changes in other joints. Three were hypertensive--one with cardiac fail- ure and tachyarrhythmia. One patient reported easy bruising. Attempting to explain the cause for the hemorrhage, Lamboley cited a mixture of local and general factors. General factors included the hemorrhagic tendency of the elderly, perhaps exacerbated by hypertension, and local factors included abnormalities of the tuber- osities and acromion secondary to rotator cuff lesions, together with tendon and synovial changes, which might cause bleeding. The osteolysis was more difficult to explain; the possible role of the hemorrhagic effusion and rotator cuff lesions were discussed.

A new chapter to the history of idiopathic destructive shoulder disease was written in 198 1 in the report by McCarty’s group in the United States of a “new syndrome” designated Milwau- kee shoulder.7 This was based on case histories of four elderly females between 63 to 90 years of

age who presented with mildly painful shoulders and clinical and radiographic evidence of rotator cuff rupture. Examination of the synovial fluid, which was blood-stained in two cases, showed

large quantities of hydroxyapatite crystals and high levels of activated collagenase in an otherwise benign-looking fluid. One patient had received several intra-articular corticosteroid injections and had been chronically taking IO mg of prednisolone for asthma, was diabetic, and had known cardiovascular disease. Another patient was hypertensive with organic heart disease, and a third had evidence of cervical radicu-

lopathy. Pathological examination in one case showed extensive osteochondromatosis of the synovium and the mineral phase was found to

consist of hydroxyapatite by the technique of energy dispersive analysis. On electron micro- scopic (EM) examination, pinocytic vesicles

were seen in fibrocytes, together with some crys- talline material. These findings led McCarty et al to postulate that hydroxyapatite crystals might escape from the site of deposition and be phagocytosed by synovial lining cells, leading to the release of collagenase and subsequent damage to the joint.13

The concept of the potential of the disease for rapid progression and destruction was extended

in a report by Lequesne et al in 1982 in Revue de Rhumatisme entitled “L’arthropathie destruc- trite rapide de l’tpaule” (ADRE; “Rapid Destructive Arthritis of the Shoulder”).’ This was defined as a rapid osteolysis of the humeral head destroying 24% to 100% of the radiographic articular surface within 6 months without evidence of any other lesion apart from degenerative changes. Their six cases of ADRE exclusively affected females between 65 and 81 years and were accompanied by previous radiographic signs of rotator cuff degeneration. In addition,

Lequesne et al reported early narrowing of the glenohumeral joint space, the appearance of transient calcific deposits in the articular region, and a variable joint effusion, which was often blood stained.

Examination showed loss of active movements, especially external rotation and abduction, rem- iniscent of rotator cuff rupture. Passive movements were affected more variably, but were often noticeably reduced during the hyperalgesic phase. This phase lasted between several months

234 CAMPION ET AL

to 2 years, after which the pain lessened and even disappeared. Radiographs showed bony destruction involving 100% of the humeral head in two patients, 50% to 70% in three, and 25% to 33% in two. Disease progression involved modifications of the humeral head, which assumed an oval appearance due to loss of the medial or supero- medial aspect. In five of six cases, calcinosis was seen, which disappeared within several weeks to months. No osteophytosis was seen, and the glenoid remained intact. Upward displacement of the humeral head was frequently seen, with evidence of erosion of the under surface of the acromion in several cases, After loss of 25% to 100% of the humeral head, the pain generally subsided, leaving some residual loss of function. Laboratory investigations were normal; the synovial fluid (blood stained in three of six cases) gave a noninflammatory picture.

In the discussion of possible etiological factors, Lequesne et al enumerated age, the presence of polyarticular disease in four of six patients, and initial involvement of the rotator cuff. Trauma was an inconstant feature, although it was felt that the intra-articular corticosteroids used in four of seven cases could have played a role- especially the use of fluorinated derivatives. They contrasted ADRE to l’epaule senile hemorrhagique, since the latter was by no means invariably destructive. Lequesne felt that their description was distinct from McCarty’s Mil- waukee shoulder, whose patients only showed mild changes secondary to rotator cuff rupture. They also felt that crystals and enzymes played little or no part in the pathogenesis of rapid destruction.

The following year, Neer et al reported 26 patients with what was described as a new syndrome, “cuff tear arthropathy.“’ However, these patients shared many of the features of previous reports: being generally elderly (mean age, 69 years), with female preponderance (20 female, 6 male), and complaining of long standing, pro- gressively increasing pain with nocturnal exacerbation, which was worsened by use and activity. Trauma was not a feature in most (20 of 26), and corticosteroids did not seem to be etiologically important. On examination, most patients had evidence of shoulder swelling, and atrophy of the supra- and infraspinatus muscles, with weakness

of external rotation and abduction. Ecchymosis was present and synovial fluid was often streaked with blood. Signs of rotator cuff disease were coupled with marked joint instability. In 14 patients, the head of the humerus could be dislocated anteriorly and posteriorly. Twelve were fixed in subluxation with stiffness and limitation of motion.

The radiological features were described as characteristic, comprising collapse of the proximal aspect of the humeral articular surface, frequent anterior and posterior dislocations, sclerosis, and small osteophytes, which developed at the point of fixed contact between the head and glenoid when this occurred. Also seen was cora- coid erosion secondary to severe erosion of the glenoid (11 patients), rounding of the greater tuberosity, reduction of the acromiohumeral dis- tance to ~2 mm, and erosion of the undersurface of the anterior third of the acromion and acromioclavicular joint.

Arthrograms were performed on all patients and all showed rotator cuff tears confirmed at operation with rupture of the supraspinatus in all 26 patients, of intraspinatus in all except one, and rupture of the long head of biceps in 18 of 26, which was frayed in a further five patients.

Laboratory tests were unremarkable; synovial fluid glucose and protein levels were normal, and the fluid was sterile on culture. Crystal and enzyme studies were not performed. It was felt that the pathological changes were due to a combination of joint inactivity, and nutritional and mechanical factors. It was postulated that rupture of the rotator cuff could lead to a leakage of synovial fluid, reducing the perfusion of nutrients to articular cartilage.

In 1984, Dieppe et al reported 12 elderly patients (11 women and one man) aged 66 to 83 years.” In addition to shoulder disease (ten cases), this group of patients was noteworthy for the presence of destructive changes affecting other joints including knees (seven), hips (three), and midtarsal joints (two).

Synovial fluid studies showed the presence of large quantities of densely staining ovoid bodies on microscopy, using Alizarin red (as described by Paul et a1,l4 confirmed as hydroxyapatite using analytical EM (four cases). Enzyme studies were not performed. This association of apa-


tite crystals with polyarticular destructive disease was named “apatite-associated destructive

arthritis (ADA)” by this group. Confirmation of the involvement of other

joints, apart from the shoulder, was subsequently confirmed by McCarty’s group.” They described a further 11 cases, seven with similar changes in knee joints. Joint fluids again contained few

leucocytes, particulate collagens types I, II, III, and basic calcium phosphate crystals (BCP) (hydroxyapatite, octacalcium phosphate, and tri- calcium phospate-one patient). Activated collagenase and neutral proteases were again found, although the results were less marked than in the

four initial cases.’ They suggested that this absence of collagenase may have resulted from recent corticosteriod injections in some instances, and a lower concentration of basic calcium phos-

phate crystals within the synovial fluid. Radiographs of the shoulders again showed

soft tissue calcification (eight of 21), glenohumeral joint degenerative changes, and rotator cuff destruction (16 of 21), which was incom- plete in a further two. Chondrocalcinosis was also observed in eight of 14 knees examined radiologically, with a striking preferential involvement of lateral tibiofemoral and patellofe-

moral compartments. Clinically, the knees showed collateral ligament instability. Calcium pyrophosphate dihydrate crystals were isolated from the synovial fluid in addition to BCP in some cases. In- four patients, histological and ultrastructural studies showed a villous structure with synovial lining cell hypertrophy giant cell formation, fibrin, and BCP crystal deposition. It was suggested that the concomitant finding of aggregates of BCP crystals together with a vir- tual absence of inflammatory cell reaction was helpful in distinguishing Milwaukee shoulder

syndrome from other common rheumatic diseases.

In contrast to the results from McCarty, collagenase has not been detected by the Bristol and Cambridge group.16 In a comparative study con- sisting of 30 females, ten each with ADA, rheumatoid arthritis (RA), and pyrophosphate arthropathy (PA), all with destructive shoulder changes, activated collagenase was detected in only three patients with RA by the diffuse fibril assay.16 It was clear that although certain clinical

and radiological features was helpful in distinguishing the three groups, much overlap was present.

IS IDIOPATHIC DESTRUCTIVE SHOULDER

DISEASE A DISTINCT ENTITY AND WHAT IS

ITS ETIOLOGY?

Certain features of idiopathic destructive

shoulder disease (IDA) appear to remain in focus: elderly patients, predominantly female, joint instability, rotator cuff rupture, voluminous blood-stained effusion, surprising passive mobility, limited pain, BCP crystals, little evidence of inflammation, marked osteolysis, and bone destruction.

Destruction of the shoulder joint may occur in RA,‘7,‘8 PA,” neuropathic arthritis,” osteonecrosis,” and septic arthritis (NA)** (Table I). Destructive joint changes have also been described in “atrophic osteoarthritis” or the so-

called analgesic hip. 23 Is IDA a distinct entity, or does it merely represent the final common pathway of a number of disease processes? Does IDA result from neuropathic, vascular, or crystal- induced inflammatory processes? In pursuit of

the answer to these questions, we are forced to

Table 1. Causes of Destructive Arthropathy of the

Shoulder in the Elderly

IDA

Neuropathic

Tabes dorsalis

Syringomyelia

Peripheral nerve injury

PA

Osteonecrosis

Avascular necrosis (post trauma)

Idiopathic osteonecrosis

Excess glucocorticoids

SLE

Hemoglobinopathies

Metabolic disease

Gaucher’s

Alcoholism

Pancreatitis

Fat embolism

Hyperlipidemia

Hyperviscosity

Bismuth intoxication

Radiotherapy

Septic arthritis

Inflammatory polyarthropathies, eg, RA

OA

236 CAMPION ET AL

recourse, once more, to the literature. Patients with RA represent a subgroup that may be distinguished on clinical, immunological, and radiological grounds,24 and will not be discussed in the following comparative approach to the literature.

Neuropathic Arthritis

In 1868 Charcot wrote: “I desire, at present, to insist upon an affection, whose existence I have pointed out, and which I am accustomed to designate, in order to prejudice nothing, by the name of arthropathy of ataxic patients.”

He reported two forms of arthropathy; the first type he named the “benignant form” in which the swelling resolved without sequelae; the second he called the malignant form where “seri- ous disorders remain in the joints, trackings, dislocations, answering to a wearing down of the osseous surfaces, and various luxations.” Despite these abnormalities, the affected limb could still be used either for walking (the lower limb) or prehension (the upper limb). He found the knee was most frequently affected, followed by the shoulder, elbow, hips, and wrists.

The pathological appearances were generally those of dry arthritis: “eburnation and deformation of the articular surfaces, deformation of the osseous extremities, bony burrs and stalactites, foreign bodies, etc.”

However, Charcot had noticed in some instances, and particularly with involvement of the shoulder “the predominance of wearing away over the production of bone burrs.” In addition, he reported the high frequency of true dislocation of the joint not seen in dry arthritis.”

Charcot was referring to a well-known chronic destructive arthropathy previously described by Mitchell in 183 1 .25 However, the association with ataxia was new. Since his time, there have been many reviews on the arthropathy that bears his name (Steindler, 193126; Key, 193227; Soto-Hall and Haldeman, 19402*; Storey, 196429; Eichen- holtz, 1 96630).

Steindler26 postulated that there are hypertrophic, proliferating, and degenerative forms. “In the latter, the degenerative changes with relaxation or displacement prevail, in the former, the hypertrophic changes, such as extra-articular and intra-articular exostoses, osteophytes and

ossification of ligaments and muscles predomi- nates.” Atrophic changes are noted, especially in the arthropathies of the shoulder and hip. “The humeral head becomes lost by attrition, the so called drumstick head.”

The presence of a large effusion, often blood- stained, is a common clinical finding. In a report by Steindler of a case with shoulder involvement he wrote: “There is a tendency to produce enor- mous effusions which dilate and perforate the capsule and penetrate into the adjacent tissues. The joint contained a great many free bodies.”

Hence, we see that many of the distinctive features of IDA become blurred when considered in the shadow of Charcot: joint instability, rotator cuff rupture, voluminous and blood-stained effusions, surprising passive mobility, limited pain, loose bodies, little evidence of inflammation histologically, marked osteolysis, and bone destruction. However, the age-sex distribution is different and most (but not all) patients with Charcot’s have neurological abnormalities, in contrast to patients with idiopathic destructive arthritis. However, neurological changes in these patients could be occult or highly localized.

Pyrophosphate Arthropathy

In 1973, Menkes et al published a series of 23 cases of destructive arthropathy in chondrocalcinosis articularis.” Of 37 involved joints, the shoulders were affected in 12. Chronic hydrar- throsis was found in 12 of 15 patients. X-ray changes were marked by joint space narrowing, subchondral cysts, osteosclerosis, and osteophytosis with partial or total destruction of the humeral head and glenoid. Erosions of the acromion were seen in six of 12 shoulders, and of the inferior part of the humeral head in some others.

Villiaumey et al encountered 37 patients with 112 joints marked by destructive changes in their series of 100 patients with chondrocalcinosis3’

In the recent series of 105 patients with PA by Dieppe et al, destructive arthritis was found in 16 of 105 patients. 32 The shoulder was involved in 36% of men and 48% of women, and was the most troublesome joint in 7% and 4%, respectively.

In all these reports the age-sex distribution of PA is not significantly different from that of our IDA patients, although the female preponder-


ante is less marked. However, radiographs show evidence of a hypertrophic response in contrast to the atrophic changes seen in IDA.

Osteonecrosis

This may affect the shoulder, but is much less common and less destructive than that involving the hip. *’ In his series of 97 patients with corticosteroid-induced osteonecrosis, Cruess found that humeral head involvement occurred in 2 1 %.33 Radiographic features are characteristic with a dense sclerotic zone adjacent to a lucent region in subchondral bone, producing the so- called crescent sign.34 There is flattening of the humeral head with no joint space narrowing for many years. Changes are restricted to the humeral head, unlike IDA, where the glenoid, acromion, and clavicle are usually involved.

uncommon.37 However, variants have been described with bone loss as the predominant feature. Erosive osteoarthritis has been described principally in distal and proximal interphalan- geal joints of the hands,38 but Utsinger et al noted humeral head erosions in three of 15 patients with this condition.39 An atrophic form of osteoarthritis has been described involving the hip (“analgesic hip”). The role of medication in this condition remains controversial, but what is seen is a rapidly destructive process occurring often with co-existing 0A.23

Current Study

Septic Arthritis

Septic arthritis of the shoulder joint is uncommon, and in the elderly it is rare for a previously normal joint to become infected.22,3s*36 Destruc- tive arthritis is an infrequent sequel to sepsis (I 2% of cases) and is manifested by gross loss of cartilage, sometimes of bone, and eventually fibrous or bony ankylosis.36

In the review of the literature of destructive arthritis of the shoulder, the history of the disease has been traced from the early reports by the French investigators to the present day. We have contrasted the clinical, radiological, and pathological changes in these described cases with other known causes of destructive shoulder disease. In addition, we have tried to emphasize the overlapping features of these diseases, in order to highlight the possibility that the shoulder joint involvement might form a spectrum of reaction of bone to a number of insults via one final common pathway.

Atrophic Osteoarthritis

Osteoarthritis is generally associated with increased bone formation (usteophytes, subchondral sclerosis), and involvement of the shoulder is

In an attempt to test this possibility, we embarked on a cross-sectional, retrospective sur- vey of patients referred to our Unit with severe shoulder disease. Our aim was to distinguish the features of IDA from features of other causes of

Table 2. Clinical Findings in 12 Patients With IDA

Ape D-

Patie”t NO. IWVSW of Svnwtrms Iv) Shoulder Pain Shoulder Examlnatio” Other Joints Comments

1 (L.V.)

2 lV.S.1

3 (R.L.)

4 MT.)

5 1K.T.)

69/F

82/F

86/F

83/F

74/F

16

5

20

9

5

Anterior dislocatian Pawlful knees

R rotator cuff ruptwed Knee elfusKms

Both shoulders unstable -

Bilateral rotatcw cuff ru~twe Both knees subluxed: elbows

Both rwtured _

Heberdan’s nodes

_ CMC disease HeLwden’s nodes

Mild untreated acramegaly 10

M

R ulnar nerve le*irms 6 lH.S.,

7 (R.T.,

6 1D.H.)

9 6i.W.)

ID (L.P.1

t t (M.P.)

76/F

76/F

75/F

66/F

81/F

64/F

9

15

6

27 Modaate/mild psi”

29 severe

ID Moderate

Knee effusicas. R knee subluxed,

unstable

K”ws unstable

Tarsal pnts involved

E‘fwion R knee

Knee POW range of “mvmne”ts.

L vwu* deformity

L knee swdle”. unstable; R knee

re.lacemant

_

Myocardial ,“‘arct

Heberden’s nodes

12 (E.G.) 82/F 5H Moderate Edateral rupture Elbows. hips. knees - _

Abbrs3htims R. rimt: L. Mt: CMC. c!mpo”w_l.

238 CAMPION ET AL

Table 3. Clinical and Laboratory Features in 50 Patients With Destructive Arthritis of the Shoulder

Clinical No. af Diagnosis Patients

F:M Ratio

Mean Disease Duration in Vrs Iranga)

No. With

POtlitive Rheumatoid

F8Ct.X

Mean Plasma Viawsih, cp (ranQel

Synovial Fluid Analysis

No. Positiie No. Positive No. of for CPPD for Apatite Mean Cell

Samples Imean suxel 1 l (mean scare) 2. Count Score 3.

RA 19 l&l 68.3 161-751 17.9 11-41) 15 I.85 (1.5-2.2) 14 0 13 (1.1) 2.4 *4

PA 16 14:2 75.1 (52.881 12.1 (l-301 0 1.76 (1.5-2.0) 14 S(1.2) 13 11.71 1.7 Idiopathic 12 12:o 77.9 (64-W 13.2 15-291 0 1.68 (1.4-2.0) 12 6 IO.81 12(1.8) 1.1 Nevopathic 3 0:3 56.0 W-78) 19.3 B-351 0 NA 2 0 0 2.0

Abbreviation: CPPD. calcium pycophosphata dihydrate.

l 1, Calcium praphfxphate dihydmte crystals. Visual scale O-3. 2. calcium hy&oxyapatite. Wsual scale O-3. 3. cell count SCQB: 0. no cells; 1, < 10’ cells/&; 2. IO”-10’ cells/&: 3.

>lOecelkf~c; 4. mean tibe 1:635 (Latex method).

destructive shoulder disease using clinical, radiological and laboratory criteria. We have presented the clinical features of 12 patients with IDA in some detail (Table 2). We also took this opportunity to review the synovial pathology of several shoulder joints that were available to us with idiopathic disease.

PATIENTS AND METHODS

Fifty patients (87 shoulders) with severe shoulder disease

referred to a rheumatology unit were included in the study.

Traumatic and soft tissue causes of shoulder disease, such as

adhesive capsulitis, were excluded. Clinical and laboratory

features were recorded including age, sex, disease duration,

plasma viscosity, and the presence of rheumatoid factor

(Latex). Where possible, synovial fluid was aspirated from

the shoulder and examined under polarized light microscopy

for the presence of calcium pyrophosphate dihydrate and

calcium hydroxyapatite crystals by Alizarin red staining”

(graded on a 0 to 3 score). The total cell count was also

estimated using a hemocytometer and recorded as follows: 0,

nil; 1, <lO’/mL; 2, lo6 to 106/ml; 3, > lo6 (Table 3).

Antero-posterior radiographs of the shoulders were

obtained and read by a single consultant radiologist (I.W.)

ignorant of the clinical diagnosis. The radiographs were

scored (on a 0 to 3 score) for the presence of various features

(see Table 4).

The underlying disease was categorised on the basis of the

full clinical, radiological, and serological examination.

Patients had RA if they met classical or definite Arthritis

and Rheumatism Association (ARA) criteria for the dis-

ease.24 All had a symmetrical polyarthritis affecting hands

and feet-Most had been strongly sero-positive for rheuma-

toid factor, and all had classical radiographic erosions. PA

was diagnosed if there was: (1) radiographic and/or synovial

fluid evidence of calcium pyrophosphate in other joint sites;

and (2) clinical evidence of joint disease at other joint sites

including knees and/or wrists or ankles; and/or (3) charac-

teristic radiographic features in other joints as described by

Dieppe and Watt,40 ie, gross flowing osteophytosis, prominent

Table 4. Radiological Features of 87 Shoulders in Patients With Destructive Arthritis of the Shoulder

Clinical Diagnosis Charcot’s Arthropathy Idiopathic PA RA

No. of shoulders examined 4 22 26 35

No. with osteophytes (mean score’) 0 7 (0.6) 15 (1.2) 6 (0.2) No. with subchondral sclerosis (mean 1 (0.2) 15 (1.2) 10 (0.6) 10 (0.4)

score’) No. with calcification 1 3 4 2

No. with periarthritis 3 (0.8) 12 (1.2) 16 (1.0) 25 (1.1)

No. with subluxation 1 (S) 12 (S) 14 KS) 17 1%

1 (I) 4 (SM) 3 6) 1 (SM)

1 dislocated 1 (MI

1 EM) No. with bony attrition (mean score’)

Acromioclavicular l(1.2) 14(1.3) 7 (0.5) 7 (0.3)

Glenohumeral 3 (1.8) 12 (1.0) 5 (0.4) 7 (0.2) Humeral head 3 (1.6) 12 (0.8) 4 (0.4) 8 (0.4) Humeral neck 2 (1.2) 8 (0.6) 1 (0) 4 (0.1)

No. with erosions 1 0 1 4

No. with osteoporosis (mean score”) 2 (0.4) 13 (0.9) 10 (0.5) 20 (1.0) No. with cysts 1 6 6 6 No. with loose bodies 3 3 3 1

No. with soft tissue swelling f effusion 1 1 1 3

Abbreviations: S, superior; I, inferior; M, medial.

*Scoring scale O-3: 0, none: 1, mild; 2, moderate; 3, severe.

DESTRUCTIVE ARTHRITIS OF THE SHOULDER

subchondral cyst formation and loose bodies, with unusual

intra-articular distribution (eg, patello-femoral involvement

in the knee). All patients in the PA group fulfilled the first criterion (i.e,

crystals present), with additional evidence of 2, 3, or both.

Patients with syringomyelia fulfilled recognized descrip-

tions of this condition.4’ IDA was diagnosed in patients with: (1) clinical evidence

of shoulder disease as shown by pain and limitation of

movement in the absence of features suggesting the diagnosis

of other rheumatological or systemic disease. (However, the

presence of OA at other joint sites did not exclude patients

from the IDA group); and (2) radiological evidence of

destructive arthritis of the shoulder joint, including destruc-

tion of bone on one or both sides of the joint line.

It was not easy to categorize all patients into the specific

groups described (RA, PA, or IDA). According to some

criteria, some or all of the PA or IDA patients could be

considered as having OA as defined by loss of joint space and

changes in subchondral bone. However, the chief differences

were the presence of chondrocalcinosis and a hypertrophic

bone response at other joint sites in the PA group, and a

relatively atrophic destructive process without evidence of

chondrocalcinosis of joints other than the involved shoulder in

the IDA group. For the purpose of this study-that is to

investigate the validity and associations of these disorders as

disease entities--each patient had to be assigned to a group.

PATHOLOGICAL STUDIES

In seven of the 12 patients with IDA, tissue obtained at surgery was examined by routine histology and EM. The mineral phase was ana- lyzed by electron microprobe. Four micron sections were stained with hematoxylin and eosin, Van Kossa for phosphates, Alizarin red for calcium, Perls for hemosiderin, MSB for fibrin and

239

collagen, and elastic Van Giessen for elastic tissue and collagen.

RESULTS

Clinical and Laboratory Studies

Patients studied included 19 with classical or definite RA, 16 with PA, and 12 with IDA affecting the shoulder (and other joints). Three patients with neuropathic shoulder destruction secondary to syringomyelia were also seen.

The clinical and laboratory features are sum- marized in Tables 2 and 3. The majority of patients were female and elderly, with long- standing disease.

CLINICAL FINDINGS

All of our patients with IDA affecting the shoulder were female and elderly (Table 2). Most had symptoms dating for many years, although many had experienced marked deterio- ration over a comparatively short period. Three patients (cases no. 7, 8, and 10) developed acute, spontaneous hemorrhagic rupture of the shoulder joint, with extensive bruising and soft tissue damage, and cases no. 7 and 8 have been reported elsewhere.42 Trauma was not a feature in most cases, apart from case no. 12 who dated severe problems in the shoulder from a fall and subsequent fracture of the humerus. Pain was generally severe and continually present in five patients. Several patients with mild or moderate

Fig knees of the bone I sublun

1. IDA of a mtis

affecting both mt with disease Marked loss of

red with lateral

240 CAMPION ET AL

pain had experienced prior episodes of more severe pain that had subsequently resolved.

On examination, there was evidence of bilateral disease in all patients. Large, cool effusions were generally present and aspiration showed voluminous amounts of frequently blood-stained fluid. Patient no. 7 had 250 mL aspirated from the right shoulder on one occasion. Shoulder movement was generally severely restricted and painful with evidence of rotator cuff rupture and marked instability (six patients). Other joint involvement was common and included knees (ten), elbows (two), hips, (one) and tarsal joints (one). In five cases (no. 4, 6, 7, 8, and ll), the affected joints were grossly unstable and radiographs showed an atrophic, destructive process similar to that involving the shoulder joint. The knee radiographs of case no. 6 are shown in Fig 1, and the remaining cases had evidence of OA. One patient had mild untreated acromegaly, and

Fig 2. RA. There is osteoporosis, erosions, and deformity of the humeral head. Some superior subluxation of the humerus due to rotator cuff disease has occurred.

one had an ulnar nerve lesion following an old injury.

The mean plasma viscosity was normal in the IDA group (1.68 cp; normal range, 1.60 to 1.72 cp), marginally elevated in the pyrophosphate group (1.76 cp), and markedly elevated in the RA group (1.85 cp). Serum from 15 of 19 RA patients gave a positive result from rheumatoid factor, and the mean titer for this group was 1 to 635. None of the other patients were seropositive in this respect.

Synovial Fluid Studies

Synovial fluid from the RA patients had a higher cell count when compared with other groups (mean, 2.4) compared with 1.7 in the PA group and 1 .l in the IDA (Table 3).

Alizarin red staining particles were seen in 13 of14RApatients,12of12IDA,and13of14PA patients; the mean score of positive fluids was 1.1, 1.8, and 1.7, respectively.

RADIOLOGY

A total of 87 shoulders were examined radiologically (Table 4). Thirty-five were from RA patients, 26 from PA patients, and 22 from IDA patients. Four shoulders were examined from NA patients. The radiological features are sum-

Fig 3. PA. Note florid hypertrophic osteophytes. subar- titular sclerosis and multiple small cysts in the humeral head. There is sliiht loss of congruity of the humerel head. No evidence of chondrocelcinosis, but pyrophosphate crystals were found in the synoviel fluid.


Fig 4. IDA of left shoulder. Note attrition of both glenoid and humeral heed in the presence of a large joint effusion. There is superior subluxation with excavation and destruction of the overlying acromion end clavicle.

marized in Table 4. Seventeen of the 19 RA patients had bilateral shoulder disease, 13 of 16 PA, and all the IDA patients. One of the three NA patients had bilateral disease. Examples are shown in Figs 2-5.

,Bone Formation

The patients in the PA group had a higher incidence of osteophyte formation than either the RA or IDA groups. Mean scores were 1.2, 0.2, and 0.6, respectively. There were no osteophytes in the shoulders of the patients with NA.

Subchondral sclerosis was most marked in patients with IDA, followed by those with PA and RA. Calcification was infrequently seen, but occurred with equal frequency in patients with PA ( 15%) and IDA ( 14%) and more commonly than in the RA group (6%). Loose bodies were uncommon, occurring in 11% of PA, 14% of IDA, and 3% of RA, but in all three NA patients.

Bone Loss

Bone attrition was most marked in patients with NA, although this group comprised only three patients. This group apart, the patients

Fig 5. NA. There is previous wiring of a pathological fracture. Note marked loss of joint space with subchondral sclerosis and early osteophyte formation. Destruction of the humeral head has occurred predominantly at its articular surface.

with IDA had a higher prevalence and severity of attrition than patients with PA or RA. The most commonly affected joint was the acromioclavicular joint, followed by the glenohumeral joints, mean score 1.3 and 1 .O, respectively, in the IDA group. Attrition of the humeral head and neck was also apparent most commonly and severely in the IDA group (0.8 and 0.6). In contrast, erosions were not often seen, but were more frequent in the RA group.

Soft Tissue Swelling

Soft tissue swelling was most frequent in the idiopathic group-being noted in ten of 22 shoulders, whereas in the RA group only three of 35 shoulders were noted to be swollen. One shoulder in each of the PA and NA groups was swollen.

Subluxation Seventy-seven percent of IDA patients had

radiographic evidence of subluxation of the glenohumeral joint-superiorly in 55%, superiomedially in 18%, and one was completely dislocated. Seventy-three percent of PA patients had subluxed shoulders-superior in 53%, inferiorly in 14%, 3% medially and superiomedially.

242 CAMPION ET AL

PATHOLOGICAL FINDINGS

Macroscopic

Synovial tissue from patients with IDA was usually hypertrophied and vascular, often with a villous structure. A few specimens were pale. Marked loss of cartilage was usual and fibrin deposition on the synovial surface and cartilage was evident. Large viscous effusions, sometimes blood stained, were found in all joints examined.

Histological sections from these patients confirmed the hypertrophic, vascular appearance of the synovial membrane seen macroscopically. Fibrin deposition was evident with fibrous orga- nization of the fibrin, in some cases with the appearance of new blood vessel formation and proliferation of fibrocytes. The most striking feature was the presence of multiple fragments of calcified material embedded both in the surface fibrin and in the cellular surface layer of the synovium itself. Synovial metaplasia was not seen. Calcification consisted both of recognizable bone flakes and granular calcified foci which stained positively with Alizarin red.

Polymorphonuclear cells, lymphocytes, and plasma cells were not in evidence; mononuclear cells were seen only in small numbers. Giant cells were occasionally present, but these were not related to calcified foci. EM and electron probe analysis confirmed the ratio of calcium and phospate of the calcified foci as typical of calcium hydroxyapatite. Some clumps of crystals differed from recognizable bone fragments by the lack of any collagen fibrils, which was characteristic of the latter.

DISCUSSION

In this review, we have traced the history of IDA of the shoulder through the literature from the earliest French reports to the present day. In an attempt to determine whether it represents a specific disease entity or the final common pathway of the response of the shoulder joint to insult, we compared descriptions of this disease process with other known causes of destructive arthritis of the shoulder. From this there emerge several features that seem to define the idiopathic group. These are elderly females with joint instability, rotator cuff rupture, voluminous blood stained effusions, reduced mobility, moderate to severe pain, BCP crystals, little evidence of inflamma-

Table 5. Comparison of Clinical, Laboratory, and Radiological Features in Different Groups of Patients

With Destructive Arthritis of the Shoulder

Feature PA NA RA IDA

Elderly

Female

Joint instability

Rotator cuff rupture

Large blood-stained effusions

Good passive mobility

Limited pain

BCP crystals

CPPD crystals

Little inflammation

Marked bony destruction

+ - + + + - + + _ + - + + + + + _ + - + _ + - - - + - - + - + +

++ - - + _ + - + + + + +

Abbreviations: +, feature present or significant: -, feature

absent or insignificant.

tion, marked osteolysis, and bone destruction. Even so, many of these features were also found in other disease processes (Table 5), and our own study on 50 patients with severe shoulder disease confirms this high degree of overlap. Unfortu- nately, there were only three patients with NA in the study, which makes analysis of the results in this group difficult. There is a striking female preponderance in the RA, PA, and IDA groups, and although the RA group were generally slightly younger than the other groups, the age distribution of PA and IDA are similar. The mean disease duration was similar for all groups. However, the RA group could be distinguished by the presence of rheumatoid factor in the serum and elevated plasma viscosity, although occasional high viscosity readings were recorded in the other groups. Interestingly, shoulder synovial fluid analysis for crystal deposits showed marked similarity between PA and IDA. Aliz- arin red staining material was frequently seen in rheumatoid patients, although in levels also seen in normals.43 The radiographic features con- tinued the theme. Osteophytosis was present more frequently and was more florid in the PA group than the IDA group. Although 17% of RA patients had osteophytosis, these were sparse and small in size. Subchondral sclerosis was most marked in the IDA group. Concurrent with the features of bone formation in the IDA group were marked features of attrition of acromioclavicular and glenohumeral joints, and the humeral head and neck. However, when severe disease occurred in individuals in all groups, distinguishing between the radiographic appear-


antes could be difficult, especially between RA and IDA.

The histological study agrees with previous

reports of a hypertrophic vascular synovium noticeable for the lack of inflammatory cell

infiltrate, and marked by the presence of multiple calcified deposits.

Attempts to define this condition as precisely

as possible is the essential first stage in under-

standing its pathogenesis. In contrast to NA, no neurological deficit has yet been discovered in our patients, although little is known about the proprioceptive and other sensory nerves innervat- ing the joint in old age, nor about the variation of sympathetic supply to blood vessels which occurs with advancing years. Similarly, the microvascu- lar network of the bone and joint is not well defined; nor are factors such as intraosseous

pressure that might affect it. Changes in the caliber and distensibility of many vessels in the

body in the elderly are well documented; how these changes affect the joint is less well known.

The attrition of subchondral bone is a striking

feature of these patients, but bone histomorphometry has not been studied. IDA could be due to the uncoupling of osteoclastic and osteoblastic activity in senile bone. It is also possible that numerous microinfarcts of bone occur, although there is no convincing evidence for this. Media- tors of bone destruction have similarly not been studied. The role of osteolytic factors such as interleukin 1 may prove to be important.

The propensity of the female sex to develop

this condition is striking. Estrogen and other hormone receptors have been found on chrondro- cytes and other connective tissue.44

BCP crystals have been identified in the synovium and synovial fluid of some of the patients, but this can be a relatively nonspecific finding.45

It is not clear whether most of the material comes from bone destruction, or whether crystal deposition is a major feature of the process. The suggestion that such particles might stimulate the generation of collagenase from synovial cells, and that this enzyme may have a central pathogenic role7 are made less likely by the inability of some workersI to find collagenase in the relevant patients. Furthermore, the extensive bone attrition would seem unlikely to be due to collagenase.

Synovial changes have been stressed by some,7

and crystal-induced cellular mitogenesis has been reported.46 Synovial inflammation of the type seen in RA or acute crystal arthropathies

has not been conspicuous in our patients, and cellular hypertrophy has been a mild, patchy phenomenon. However, a synovial role in the pathogenesis cannot be excluded.

A primary immunological process seems

unlikely in view of the lack of any lymphocytic or plasma cell accumulation in either the synovial fluid or tissues, as well as the lack of any obvious

immunological abnormalities or acute phase response in the blood.

What is the relationship between IDA and OA? Erosive changes in the shoulder have been

reported in association with erosive 0A.27 It is also clear from the literature that destructive changes may occur in the hip in association with 0A.23 Similar changes are seen in out patients, both in the hips and at other joint sites, such as

the shoulder and knee. Evidence of OA was common in the IDA group. The results of the clinical, laboratory and radiological studies reflect a high degree of overlap, especially between the IDA and PA patients. The RA patients were more easily distinguished by the presence of a systemic inflammatory disease,

classical rheumatoid erosions, and rheumatoid factor, although when the shoulder joint was

taken in isolation, even distinguishing between the rhematoid patients was not straightforward. Therefore, we postulate that it is unlikely to be

helpful to assign PA, IDA, and OA to diagnostic groups. What we are witnessing is a spectrum of disease within OA with the presence of crystals pointing to different modifying factors.

What positive conclusions is it possible to make about the nature of IDA? The etiopatho- genesis must involve an age-related phenomenon with a predilection from the female sex. The lack of a local or systemic inflammatory response suggests that the synovium may not be primarily involved but that a disorder of bone is most likely. Although the shoulder is the most frequently involved joint, the fact that other joints may be involved suggests that it may be a systemic disorder. The fact that bony attrition can occur well away from the joint capsule supports this hypothesis. It is clear that progress in this field will depend on a multidisciplinary approach involving long term prospective studies, detailed

244

pathological examination of synovium and bone, involving histomorphometry as well as ultrastructural studies.

SUMMARY AND CONCLUSION

IDA of the shoulder is a condition found predominantly in elderly females. Although the shoulder is primarily involved, other joints such as the hip and knee can be affected, and concurrent OA is common at other joint sites. Clinical features include voluminous, often blood-stained effusions, together with features of rotator cuff rupture and restriction of shoulder movement. Laboratory parameters are usually normal and examination of the synovial fluid reveals large amounts of basic calcium phosphate crystals. The synovium is hypertrophied and vascular and shows fibrin deposition. It contains calcified material extracellularly. An acute inflammatory infiltrate is absent. Radiographs demonstrate soft tissue swelling and subchondral sclerosis

CAMPION ET AL

with marked bony attrition involving the acromioclavicular and glenohumeral joints, as well as the humeral head and neck. Although some aspects of the disease seem distinct, many features are shared with other types of destructive arthritis of the shoulder.

The pathogenesis of this disorder is at present obscure, but it is clear that an understanding of the processes involved will provide a vital contri- bution to our understanding of the response of the joint to insult. With a multidisciplinary approach and adequate communication between interested workers this aim could seen be within our grasp.

ACKNOWLEDGMENT

Our grateful thanks are due to the Arthritis and Rheuma-

tism Council for financial support, Dr M. Doherty for his

help with cases, J. Hornby and A. Swan for their work in

laboratory analysis, and Margaret Clarke for her tireless help

with the typing.

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Idiopathic Destructive Arthritis of the Shoulder

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