Solitary Osteochondroma of the Ventral Scapula Associated with Large Bursa Formation and Pseudowinging of the Scapula: A Case Report and Literature Review

Osteochondroma (OC) is the most common benign bone tumor and may occur on any bone in which endochondral ossification develops. Although scapular OC accounts for less than 5% of the cases of solitary OC, OC is the most common lesion among the tumors and tumor-like lesions of the scapula. OC that develops near the medial scapular border easily causes friction with the ribcage; hence, almost half the number of cases of OC associated with marked bursa formation develops in the ventral scapula. We report a case of a 27-year-old female with a painful OC of the ventral scapular surface associated with large bursa formation and pseudowinging of the scapula. After l2 years of follow-up with magnetic resonance imaging, we confirm that the accompanied bursa left at surgery disappears.


Introduction
Osteochondroma (OC) is the most common benign bone tumor, of which the detailed development process is still debatable. e reported incidence of OC is 33-35% of benign and 8-10% of all surgically removed bone tumors, which may be an underestimation as most OCs are asymptomatic and are never found [1,2]. OC may occur on any bone in which endochondral ossi cation develops. e most common sites of OC development are the metaphyseal region of the long bones of the limbs, while at bones are less commonly involved [2]. Symptoms often develop in relation to the size and location of the OC lesion. Pain may result from fracture, bursa formation, arthritis, and impingement of adjacent tendons, blood vessels, nerves, or the spinal cord [1,2]. We describe a case of a 27-year-old female with a painful OC on the ventral surface of the scapula associated with a large bursa and pseudowinging of the scapula with l2 years of follow-up. Written informed consent was obtained from the patient for publication of this case report and accompanying images. A 27-year-old right-hand-dominant and otherwise healthy female student presented with a pain in the right upper scapular region that increased with shoulder motion and resting in the supine position. She reported that a painless snap in her back had occurred during sports activity 11 years previously and had disappeared 2 years later after discontinuing sports activity. e pain in the right upper scapular region had appeared 3 months earlier during continuous inputting to her personal computer and had rapidly worsened. She presented at a nearby hospital because the pain was generated during activities of daily life and prevented her from sleeping in the supine position. A physician suspected a malignant bone tumor based on radiographic and magnetic resonance imaging (MRI) ndings and referred the patient to our hospital. e patient had no relevant family or medical history. e right shoulder was slightly lower than the contralateral shoulder. ere were no neurological de cits in the right shoulder or arm. ere was winging of the right scapula with the arm at the side. An upper interval between the spine and the medial scapular border was widened by 70%, but the lower one was not ( Figure 1). ere was no atrophy of the back muscle, and contraction of the trapezius was normal. e muscle bellies of the short rotators and rotator cu were not tender and were without defects. e limitations of the active ranges of motion were 10°for total elevation, 15°for external rotation, and two vertebrae for internal rotation. Horizontal adduction was not limited with moderate pain beyond 100°. e empty can test generated upper scapular pain. No deformity or osseous tumor was palpable in the large joints, pelvis, or ribcage. Radiographs revealed a bone mass extruding from the ventral side of the superomedial scapular angle; no abnormality was depicted in the large joints. Computed tomography showed a mushroom-shaped osseous tumor composed of a cortex continuous with the scapular cortex, with a broad at distal end that almost contacted with the third rib, as well as a soft tissue tumor between the serratus anterior and the ribcage (Figures 2(a) and 2(b)). MRI taken at the previous hospital revealed a cystic lesion containing a large amount of uid that surrounded the osseous tumor and spread over the upper two-thirds of the scapula (Figures 3(a) and 3(b)). Marked rim enhancement was demonstrated on contrast-enhanced T1-weighted imagery with fat suppression. From these imaging ndings, our diagnosis was a solitary OC with a large bursa; the possibility of malignant transformation was considered to be low.

Case Report
We performed surgery 3 months after the patient's rst visit to our hospital. Under general anesthesia, the patient was placed in the lateral decubitus position with the shoulder exed and abducted at 110°. e upper extremity was supported on a pillow to avoid excessive horizontal adduction so that the superomedial scapular angle was situated just underneath the middle trapezius. A 10 cm longitudinal incision was made along and 3 cm medial to the medial scapular border, centering at the most proximal end of the scapular spine. e trapezius and rhomboid minor were divided along their bers. e thick and edematous cyst wall exposed in the bottom of the operative eld was cut, and about 100 ml of clear yellow-brown uid owed out. e stalk of the OC arose in the superomedial scapular angle 1 cm lateral to the medial scapular border and penetrated the subscapularis and serratus anterior muscles. e base of the lesion was cut with its periosteum along the ventral scapular surface. We cut the attached thick brous tissue attached around the distal stalk, which was considered to be a bursal wall. After resection of the osseous lesion, a large cystic space appeared, covered by a white thick membrane considered to be in amed synovial tissue; at the bottom of this space a 1 × 3 cm section of the rib surface was exposed in the defect of the thick membrane ( Figure 4). ere was no free body in the space or palpable indurations on its wall. We irrigated the space, sutured the fascias of the divided muscles, and subsequently closed the skin.
Macroscopically, the typical thick perichondrium and cartilage cap were not found, although the at distal end of the lesion was covered by spotty brocartilage-like tissue ( Figure 5). Histological examination revealed characteristic ndings of OC without any malignant changes. e distal end was covered by synovial tissue and was composed of bony trabeculae in which mostly fatty tissue and bone marrow intervened. e postoperative course was uneventful. e patient returned to normal daily life and full activity 3 weeks postoperatively. At the time of nal follow-up 12 years postoperatively, the right scapula was in the normal position, the scapulothoracic rhythm was symmetrical, and there was no limitation of active range of motion or any associated crepitus. e Constant score ratio compared with the contralateral left shoulder was 100% [3]. MRI showed no abnormality of the soft tissue or bony structures ( Figure 6).

Discussion
OC is the most common benign bone tumor [1,2]. It has been reported that 14% of OC are hereditary multiple OC  After resection of the osseous lesion, a large cystic space appeared, covered by a white thick membrane; at the bottom of this space, a 1 × 3 cm section of rib surface covered by edematous synovium was exposed in a defect of the thick membrane.
(an autosomal-dominant disorder) and 86% are solitary OC without heredity [1,4]. Solitary OC is a common lesion estimated to occur in 1-2% of individuals [4]. e literature indicates little sex predilection [1]. e cartilaginous cap is the site of active growth, and the degree of maturity parallels the host bone. If the OC is arrested, as may occur in adults, there may be practically no cartilaginous cap. is appearance is especially likely with the rare OC associated with an overlying bursa [1]. In a minority of cases, OC may grow beyond skeletal maturity [5].
e lesion in our case was a solitary OC, as the physiological and radiographic investigations found no other bony abnormalities. e OC was considered to be arrested, as there was no cartilaginous cap histologically.
e most common sites of involvement are the metaphyseal region of the long bones of the limbs, while involvement of at bones is less common [2]. e scapula is reportedly the site of occurrence of 1-3% of all primary bone tumors [6]. OC is the most common of the tumors and tumorlike lesions of the scapula, accounting for 17-40% [6,7]. e majority of scapular tumors are of cartilaginous origin; this may be because the scapula develops by endochondral ossication from seven ossi cation centers and has a total length of physes exceeding any tubular bone [6]. Scapular lesions account for 4-4.9% of the solitary OC cases [1,4]. e vast majority of OC are asymptomatic. Symptoms are often related to the size and location of the lesion [2]. e most common symptom is a nontender, painless cosmetic deformity related to the slowly enlarging mass. Additional complications that cause pain include fracture, bursa formation, arthritis, and impingement of the adjacent tendons, blood vessels, nerves, or spinal cord [1,2,4]. Approximately 60-80% of patients with OC were younger than 20 years at the time of the rst excision of the OC [1,4]. Although it is uncommon for a solitary OC to become symptomatic after skeletal maturity, there are some well-documented reports of the appearance of symptoms in adults that resulted from the following: mechanical irritation of muscle, tendon, or soft tissue; compression of a nerve; formation of a pseudoaneurysm or an adventitious bursa; fracture; infection; ischemic necrosis; or malignant transformation [8]. In our case, the symptoms appeared after skeletal maturity.
In 1891, Orlow [9] originally described the bursa formation between an OC and the surrounding soft tissue as "exostosis bursata," although this had been recognized previously. e exact occurrence rate of bursal formation associated with OC is unknown, but Unni and Inwards [1] stated that an overlying bursa was signi cant enough to be described in 1.3% of their cases treated surgically. McWilliams [10] reported the rst case of ventral-side scapular OC accompanied by adventitious bursa. Since this rst reported case, to the best of our knowledge, there have been 20 cases of the solitary ventral-side scapular OC associated with a large bursa (including our case) reported in the English literature (Table 1). e scapula glides over the thoracic wall, cushioned from the undulating surface of the ribs by the serratus anterior and subscapularis muscles. However, the scapular superior and inferior angles, and its medial border, are relatively poorly cushioned [11]. Endochondral ossication occurs at the medial border and lateral angle of the scapula, where OC commonly develops. OC near the medial scapular border then easily causes friction with the ribcage. In the literature, 41-73% of OC associated with marked bursa formation are located on the ventral scapula [4,[12][13][14]. Many authors described that the scapular OC with a large bursa penetrated the subscapularis and serratus anterior muscles and that the bursae were formed along the chest wall; although Chiarelli et al. reported an OC case associated with intramuscular bursa formation in the serratus anterior [15]. It remains unknown whether the bursa associated with the OC in our case was an adventitious bursa or an in amed consistent bursa located between the serratus anterior and the ribcage [16]. ese bursae associated with OC are lined by synovium and may hemorrhage or become in amed or infected. In addition, the bursa may contain chondral or brin bodies, and chondrometaplasia can occur within the synovial lining, leading to secondary synovial chondromatosis [4,14,[17][18][19][20]. In our case, there was no free body in the bursa and no palpable induration on the bursal wall that would have indicated chondrometaplasia or secondary osteochondromatosis. Traces of direct contact between the lesion and the ribs were apparent, and the bursa was formed between the serratus anterior and the chest wall.
ese ndings are consistent with other reports that  described the existence of resorption or erosion of the contacting ribs [21,22]. Scapular winging and snapping have been well recognized as symptoms of OC development on the ventral scapula. e causes of scapular winging are numerous. Increased scapular prominence from causes other than paralysis of the serratus anterior muscle is referred to as "pseudowinging" of the scapula [23]; this pseudowinging often leads to the discovery of OC on the ventral scapula. Of the 20 reported cases of ventral scapular OC (including our case), 14 cases showed pseudowinging (Table 1). e types of winging indicate the developing location of the OC, although they are characteristically present even at rest with the arm at the side. Carlson et al. [24] analyzed the etiologies of the snapping scapula syndrome causing shoulder discomfort characterized by painful, audible, and/or palpable abnormal scapulothoracic motion in 89 reported cases. ey found that the most common causes of snapping scapula syndrome were skeletal abnormalities (43% of reported cases), of which three were OC. Of 20 reported cases of ventral scapular OC (including our case), 14 cases had symptoms consistent with snapping scapula syndrome (Table 1). erefore, snapping scapula is a common symptom in cases of ventral scapular OC, although OC is an uncommon cause of snapping scapula.
Malignant transformation of OC is well known. WHO reported that the risk of malignant transformation to secondary peripheral chondrosarcoma is estimated at about 1% for solitary and up to 5% for multiple OC [2]. Some authors reported that 27.3-36.3% of patients with multiple OC who underwent surgery had secondary chondrosarcoma, whereas only 3.2-7.6% of patients with the solitary form had malignant changes [1,25,26]. Nevertheless, follow-up studies in a number of patients with multiple hereditary OC revealed that malignant change occurs in less than 1% of patients [27]. Secondary chondrosarcoma in OC reportedly has a predilection for at bones [26]. Clinically, malignant transformation should be suspected in lesions that grow or cause pain after skeletal maturity, as OC only rarely enlarges after this time [4]. e most frequent imaging ndings of malignant transformation are irregularity or indistinctness of the surface of the OC, areas of lucency and inhomogeneous mineralization within the OC, and a soft tissue mass frequently containing foci of scattered, punctuate calci cations [26]. On MRI, malignant transformation should be suspected in large tumors with cartilaginous caps that are thick (>1.5-2 cm in an adult) and unmineralized [2]. However, di erentiation between the uid in the in amed bursa and a large cartilaginous cap is di cult, as they have similar signal characteristics on MRI [5]. In our case, there were no characteristic radiographic ndings that indicated malignant transformation. e existence of a thick cartilaginous cap was almost de nitively ruled out preoperatively, as the interval between the distal end of the OC and the opposite ribs was 2-3 mm. Histopathological examination con rmed that there were no malignant ndings and no cartilaginous cap.
In the approach for OC on the ventral side of the superomedial scapular angle, the superior bers of the trapezius must be separated. is approach carries a risk of harm to the spinal accessory nerve, which travels an average of 2.7 cm lateral to the superomedial scapular angle [16]. To minimize this risk, Case Reports in Orthopedics we placed the patient in the lateral decubitus position with the shoulder exed and abducted at 110°, so that the superomedial scapular angle was situated just underneath the middle bers of the trapezius. An operative eld large enough to remove the OC was gained, but it was impossible to observe the whole interior of the associated bursa. We left the bursa untouched to avoid damaging the long thoracic and dorsal scapular nerves that travel closely along the bursal wall. Of the 19 previously reported cases of ventral scapular OC, complete resection of the bursa was performed in eight cases and partial resection was done in two. Regarding treatment of the bursa, there are two di erent opinions: one that total resection has to be performed [13] and one that aggressive resection of the bursa is unnecessary as the bursa should not recur once there is no longer irritation of the underlying ribs [22]. Some authors have reported success with no or partial resection of the bursa [22,28,29]. e bursa accompanying OC involves in ammation caused by mechanical irritation, which produces excess synovial uid. When the mechanical irritation disappears, the in ammation resolves and the bursal tissue should be normalized. In our case, MRI taken at the time of nal follow-up 12 years postoperatively showed no abnormality of soft tissue. erefore, the bursa itself may resolve when there is no osteochondral free body and indurations in the bursal wall. Arthroscopic excision recently developed for symptomatic OC is e ective if the OC is de nitely benign [29].

Consent
Written informed consent was obtained from the patient for the publication of this case report and accompanying images.