Secondary osteochondromatosis in the subacromial bursa: a report of two cases and review of the literature

J Orthop Sci (2004) 9:317–322 DOI 10.1007/s00776-004-0778-3

Secondary osteochondromatosis in the subacromial bursa: a report of two cases and review of the literature Jun’ichiro Hamada1, Kazuya Tamai2, and Koichi Saotome2 1 2

Kuwano Kyoritsu Hospital, 2-9-18 Shima, Koriyama 963-8034, Japan Department of Orthopaedic Surgery, Dokkyo University School of Medicine, Tochigi, Japan

Abstract Osteochondromatosis is classified into primary and secondary lesions; primary osteochondromatosis is a tumorlike lesion, whereas secondary lesions are due to such joint or bursal disorders as osteoarthritis and osteochondral fractures. There is no clinical distinction between these two conditions. Only the pathological findings of loose bodies and synovium can clearly distinguish between them. In this report, we present two patients with secondary osteochondromatosis in the subacromial bursa. Both had shoulder pain and were treated surgically. We discuss methods of differentiating between primary and secondary lesions and elucidate the pathogenesis of osteochondromatosis in the subacromial bursa by analyzing findings for 17 shoulders with this condition reported in the literature. We also present two more cases. We reviewed the 12 cases of osteochondromatosis in the literature for histopathological findings of loose bodies and the presence or absence of acromial osteophytes. Our findings suggest that osteochondromatosis of the subacromial bursa is secondary in most cases, and that osteocartilaginous fragments from acromial osteophytes can be shed into the subacromial bursa and grow into loose bodies. Key words Secondary osteochondromatosis · Subacromial bursa · Pathogenesis

Introduction Osteochondromatosis in the subacromial bursa is rare; only 14 such cases have been reported to date.1–4,6,8,10–14,16,17 As for synovial osteochondromatosis in a joint, osteochondromatosis in the subacromial bursa may be primary or secondary. However, few of the previous reports referred to the differential diagnosis between primary and secondary lesions.8 We examined loose bodies removed from two patients who had osteochondromatosis in the subacromial bursa, with Offprint requests to: J. Hamada Received: August 15, 2003 / Accepted: January 28, 2004

special reference to whether the disease was primary or secondary. We discuss methods of differentiating between primary and secondary lesions and elucidate the pathogenesis of osteochondromatosis in the subacromial bursa by analyzing findings for 17 shoulders with this condition in the literature and the present two cases.

Case reports Case 1 A 54-year-old man visited our clinic on May 10, 1996 with a 3-year history of intermittent aching discomfort and deltoid muscle snapping in the right shoulder joint. He had undergone surgery of the right shoulder with a diagnosis of osteochondromatosis at another hospital in 1992, at which time 35 loose bodies were removed from the subacromial bursa. On our examination, he had slight restriction of motion in the right shoulder joint but no muscle atrophy; no impingement signs or painful arc signs were elicited. A popping sensation was palpated over the middle deltoid when he swung the arm forward and backward. Plain radiographs revealed several radiopaque lesions underneath the acromion and osteophytes on the undersurface of the acromion and at the greater tuberosity (Fig. 1). Arthrography revealed a joint-side tear of the rotator cuff. Diagnostic arthroscopy performed on June 24, 1996 revealed normal articular cartilage and slight proliferation of the synovium without a cartilage mass. There were no loose bodies in the glenohumeral joint. Open surgical exploration of the subacromial bursa revealed six loose bodies in the proliferated bursal wall. We removed all of them (Fig. 2) as well as the acromial osteophyte and most of the subacromial bursa. In addition, we made certain that the osteophyte of the greater tuberosity produced snapping of the deltoid muscle and

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Fig. 3. Histology of a loose body (decalcified material). Histologic section of a loose body demonstrating lamellar bone (arrow), a new cartilage layer (arrowhead), and superficial loose connective tissue. H&E Fig. 1. Anteroposterior radiograph of the right shoulder joint. Some radiopaque nodules are present in the subacromial space and greater tuberosity (arrow). Osteophytes are seen on the undersurface of the acromion and the greater tuberosity

Fig. 2. Six loose bodies removed from the subacromial bursa

then removed it. Histological examination of the loose bodies revealed lamellar bone enveloped with loose connective tissue (Fig. 3). Nonspecific inflammation was found in the bursal membrane (Fig. 4). No irregular nests indicating a primary lesion were noted in any of the specimens. Immunohistochemical localization with antibody to proliferative cell nuclear antigen (PCNA) was performed using the ABC immunoperoxidase method. Few nuclei of chondrocytes were stained by the PCNA, whereas many fibroblasts stained in the surrounding soft tissue (Fig. 5). The subacromial bursa exhibited nonspecific inflammation, but no irregular nests were found. Follow-up radiographs revealed no recurrence of loose bodies. The patient has been pain-

Fig. 4. Histological section of the subacromial bursa shows nonspecific inflammation

Fig. 5. Chondrocytes and surrounding soft tissue. Few nuclei of the chondrocytes were stained in contrast to many fibroblasts in the surrounding soft tissue. PCNA ⫻100

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Fig. 7. Eight loose bodies removed from the subacromial bursa

Fig. 6. Anteroposterior radiograph of the left shoulder joint. Some radiopaque nodules are present in the subacromial space and just below the glenohumeral joint (arrows). Osteophytes are seen on the undersurface of the acromion and the greater tuberosity

free with normal shoulder function for the 7 years following surgery. Case 2 A 51-year-old man visited us on March 27, 1996 with a 3-day history of pain and dullness in the left shoulder joint. He had experienced, although only occasionally, a catching sensation in the same shoulder. On examination, there was atrophy of the spinati muscles and tenderness over the greater tuberosity, although all ranges of motion were nearly normal. Signs of impingement and the painful arc sign were absent. Radiographs of the left shoulder joint revealed calcifications underneath the acromion and inferior to the glenohumeral joint. Osteophytes were noted on the undersurface of the acromion and over the greater tuberosity (Fig. 6). Magnetic resonance imaging (MRI) revealed a fullthickness tear of the rotator cuff. On January 13, 1997 his shoulder was explored. Because arthroscopy of the glenohumeral joint revealed only proliferation of the synovium and fibrillation of articular cartilage, open surgery was performed. We retrieved eight loose bodies: three from the subacromial bursa and five from the subcoracoid bursa (Fig. 7). We also excised the inflamed subacromial bursa but did not repair the torn cuff because it did not appear to be a cause of his shoulder pain. Histological examination of

Fig. 8. Histological section of a loose body demonstrating lamellar bone (arrow), calcified cartilage (arrowhead), and superficial loose connective tissue. H&E

Fig. 9. Histological section of the subacromial bursa shows nonspecific inflammation

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Fig. 10. Chondrocytes and surrounding soft tissue. Few nuclei of chondrocytes were stained in contrast to many fibroblasts stained in the surrounding soft tissue. PCNA ⫻100

the loose bodies revealed nidi consisting of necrotic lamellar bones, whereas no irregular nests indicating a primary lesion were found (Fig. 8). The bursa revealed nonspecific synovitis, but no nests of proliferating cartilage were seen (Fig. 9). PCNA staining showed the same findings as in case 1 (Fig. 10). Six years postoperatively, he is free from pain and the catching sensation while practicing judo. There has been no radiological evidence of recurrence.

Discussion Synovial chondromatosis (or synovial osteochondromatosis) was first clearly defined by Jaffe5 as a condition developing in the synovial membrane through metaplasia. Milgram7 stated that the process of this condition included three phases: (1) intrasynovial disease only, with no loose bodies; (2) transitional lesions with both intrasynovial proliferation and free loose bodies; and (3) multiple loose bodies without demonstrable intrasynovial lesions. Articular loose bodies can be of various origins, such as from osteochondral fractures and osteoarthritis.9 For this reason, a combination of surgical findings of free loose bodies and a histopathological absence of intrasynovial lesions, as in both of our patients, does not always indicate phase 3 synovial (or bursal) chondromatosis. Villacin and colleagues18 clarified the histopathological differences between the primary and secondary synovial chondromatosis of Jaffe.5 In primary disease, loose bodies and cartilage nodules in synovium exhibit irregular nests with frequently binucleated cells formed by metaplastic cartilage and patchy diffuse calcification. In contrast, in what Villacin et al. classified as secondary lesions, calcifications are zonal and “ring-like,” with uniform chondrocytes evenly distributed; moreover, fragments of articular cartilage or subchondral bone may be present at the center of loose bodies. They also

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stated that these histopathological findings were associated with the clinical course: Postoperative recurrence was encountered in 6 of their 10 patients with primary lesions, whereas none of the 126 patients with secondary lesions suffered recurrence.18 One of us (K.S.)15 has already reported that the phase 3 disease of Milgram should not be regarded as the natural course of primary synovial chondromatosis but, rather, should be diagnosed as primary or secondary employing the criteria of Villacin et al. On the basis of histopathological findings, the most reasonable diagnosis for both of our cases is secondary osteochondromatosis, or secondary chondrometaplasia according to the criteria of Villacin et al.18 K.S. also revealed that numerous nuclei of chondrocytes in loose bodies were stained by PCNA in primary synovial chondromatosis, in contrast to the few nuclei seen in secondary osteochondromatosis.15 These findings suggest that loose bodies have the potential for growth via proliferation of chondrocytes in primary osteochondromatosis and via metaplasia following proliferation of surrounding connective tissue in secondary osteochondromatosis. Low PCNA immunoreactivity of chondrocytes and high PCNA immunoreactivy of fibroblasts in our cases shows that they can be diagnosed as secondary osteochondromatosis. The mechanism of loose body formation in our patients is a matter of interest. Unlike the glenohumeral or other joints, the normal subacromial bursa does not have cartilaginous or osseous structures exposed in its cavity. This was particularly true in case 1, in which there was no full-thickness cuff tear and therefore no communication between the joint and the bursa. However, the subacromial bursa wall is usually tenacious, with the coracoacromial ligament positioned superiorly and the rotator cuff and greater tuberosity inferiorly. Acromial osteophytes are formed at the acromial end of the coracoacromial ligament so that, with mechanical impingement, small ossified or nonossified particles may separate from the growing osteophyte and enter the bursal cavity via an injured portion, or they may migrate through the bursal wall. These particles may be nourished with synovial fluid, and some of them may develop into loose bodies. Although there is no direct evidence that loose bodies are derived from osteophytes, lamellar bone found as nidi in loose bodies show that they originate from osteophytes at the acromion or the greater tuberosity (Figs. 3, 8). Histological findings of loose bodies indicate their origin and process of growth.9 The mechanism by which small ossified particles shed from osteophytes migrate into the subacromial bursa is still unclear. We observed radiographically that calcified deposits in the rotator cuff are extruded into the subacromial bursa. The subacromial bursa may be a

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Table 1. Characteristics of patients reported in the literature and the two present cases Study Symeonides17 Sim16 Numajiri13 Nakano12 Sakanishi14 Milgram8 Nakagawa11 Hirose2 Honjyo3 Ko6 Fujii1 Morii10 Ishikawa4 Present case 1 Present case 2

Age (years)

Sex

Acromial osteophytes

Cuff tearing

Pathological diagnosis

41 35 59 72 37 36 61 40 37 70 46 68 47 47 52 54 51

M M M M M M M M M F F F M M M M M

Unclear Unclear ⫺ ⫺ ⫹ ⫺ ⫹ ⫹ ⫺ ⫹ Unclear ⫹ ⫹ ⫹ ⫺ ⫹ ⫹

Unclear Unclear ⫺ ⫺ ⫹ (incomp.) ⫺ ⫹ (comp.) ⫺ ⫺ ⫺ ⫹ (comp.) ⫺ ⫹ (incomp.) ⫹ (incomp.) ⫺ ⫹ (incomp.) ⫹ (comp.)

Unclear Unclear Primary Primary Primary Secondary Secondary Secondary Secondary Secondary Secondary Secondary Secondary Secondary Secondary Secondary Secondary

Primary: primary osteochondromatosis; Secondary: secondary osteochondromatosis; comp.: complete cuff tear; incomp.: incomplete cuff tear

space surrounding the shoulder joint for phagocytosis of unnecessary materials such as small ossified or cartilagenous particles and calcium phosphate. We suspect that osteophytes at the acromion or the greater tuberosity occasionally suffer microfractures (e.g., asymptomatic microfracture of intraarticular osteophytes). Because these small fractured particles can migrate into the subacromial bursa and be absorbed by macrophages, we rarely encounter the case of osteophyte fracture or extrabursal osteochondromatosis. In case 2, in which a full-thickness cuff tear was present, the possibility cannot be excluded that the loose bodies initially arose in the glenohumeral joint and then moved to the subacromial-subcoracoidal bursa. To elucidate further the pathogenesis of osteochondromatosis in the subacromial bursa, we analyzed findings for 17 shoulders in 16 patients with this condition reported in the literature and present another two cases (Table 1). Based on the histopathological criteria of Villacin et al., primary disease was recognized in 3 shoulders and secondary disease in 12; the diagnosis was indeterminate for 2 shoulders. The presence of a number of loose bodies indicates primary disease of the subacromial bursa; fewer loose bodies indicate secondary disease because there are fewer shed particles from osteophytes. Rotator cuff tear was observed in seven shoulders: full-thickness in three and partial-thickness in four. No full-thickness tear were observed in three shoulders with a primary lesion. Therefore, the presence of a full-thickness tear, which in theory may result in production of loose bodies from the glenohumeral joint, was not related to the primary lesion.

Acromial osteophytes were observed in 8 of 12 shoulders with a secondary lesion. This appears to support the hypothesis that the shedding of fragments from acromial osteophytes into the bursal cavity is a likely cause of secondary osteochondromatosis in the subacromial bursa. This hypothesis may be criticized using the argument that if it is true, loose bodies in the subacromial bursa would be encountered more frequently in orthopedic practice. We believe that most of the fragments shed from acromial osteophytes are captured in the bursal synovium and are resolved by cells including macrophages. However, under what conditions free fragments grow into recognizable loose bodies in the subacromial bursa remains a subject for future study.

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