Copyright

1982 by The Journal

of Bone and Joint Surgery, incorporated

Subacromial Bursography
AN ANATOMICALANDCLINICAL STUDY* BY ALAN M. STRIZAK, M.D.t, TORRANCE,LARRYDANZIG, M.D.t, SAN DIEGO, DOUGLASW. JACKSON, M.D.,LONG BEACH, GUERDONGREENWAY,M.D.1, DONALDRESNICK,M.D.**, SAN DIEGO, AND TOMSTAPLE, M.D.tt, LONG BEACH, CALIFORNIA
From the Veterans Administration Hospital, San Diego, and the Memorial Hospital Medical Center, Long Beach

ABSTRACT: Impingement of the rotator cuff be neath the coracoacromial arch without associated rup ture of the cuff or reactive bone changes on the undersurface of the acromion is a well established clinical diagnosis. The value of subacromial bursography in the assessment of this condition was investigated in an anatomical study of fifteen cadavera and a clinical study of thirty-one patients. The subacromial bursa is situated like a cap over the rotator cuff and can be demonstrated roentgenographically by the injection of contrast material in shoulders from cadavera and living subjects. This bursa is composed of subacromial and subdeltoid portions as well as a subcoracoid extension in some in dividuals. However, it is the anterior portion of the bursa, under the coracoacromial arch, that is most significant, since this overlies the deep structures in volved in the impingement syndrome. The normal sub acromial bursa easily accepts five to ten milliliters of contrast medium. However, if the bursal walls are thickened and edematous, the bursa will be difficult to demonstrate roentgenographically or it will accept only a few milliliters of contrast material. The findings in this study suggest that when the findings on the bursogram are normal, a diagnosis of chronic impingement by the coracoacromial arch should be questioned.
The subacromial bursa is the largest bursa in any ex tremity of the human body, yet subacromial bursography has been neglected as a way to investigate pain and disa bility of the shoulder. It is well established that secondary filling of the subacromial bursa at the time of shoulder ar* Supported in part by Veterans Administration Grant 7406. t Orthopedic Division, Harbor-University of California at Los Angeles Medical Center, 1000 West Carson Street, Terranee, California 90509. Please address reprint requests to Dr. Strizak. Division of Orthopedic Surgery, Veterans Administration Hospi tal, 1200 North Tustin Avenue, Santa Ana, California 92905. Sports Medicine Clinic, Memorial Hospital Medical Center of Long Beach, Long Beach, California 90801. 71 Department of Radiology, Baylor University Medical Center, Dallas, Texas 75246. ** Department of Radiology, Veterans Administration Medical Center, 3550 La Jolla Village Drive, San Diego, California 92161. tt Department of Radiology, University of California, Irvine and Memorial Hospital Medical Center, Long Beach, California 90801.

thrography confirms a full-thickness disruption of the rotator cuff. In the absence of disruption of the cuff, how ever, the subacromial bursa does not fill with contrast ma terial during opacification of the glenohumeral joint2-7"
9,13,14,17

The subacromial bursa is a consistently present, well defined, thin-walled structure that sits atop the rotator cuff like the cap of a mushroom or a beret. Normally there is some variation in the shape of the bursa, depending on the extent of the development of its subdeltoid, subacromial, and subcoracoid portions1. Secondary changes in the sub acromial bursa, such as edema and adhesions, are thought to be associated with rotator-cuff injuries and coraco acromial impingement3. There are few objective tests available for the diag nosis of pain syndromes of the shoulder in athletes. Sub acromial bursograms give reproducible results that can provide further insight into chronic changes in the struc tures under the coracoacromial arch. This test appears to be of value in assessing the impingement pain syndrome and in differentiating it from subtle instability of the glenohumeral joint and intrinsic rotator-cuff disease. This report describes the anatomy of the subacromial bursa, the technique of its opacification, and the application of this technique to the evaluation of impingement syndromes of the shoulder.

Anatomical Study
The normal anatomy of the subacromial bursa was studied using subacromial pneumobursography, double glenohumeral arthrography, and latex injections of the bursa in adult fresh cadaver specimens. These studies were carried out by three of us (L. D., G. G., and D. R.) at the Veterans Administration Hospital, San Diego, California.

Materials and Methods

Twenty fresh cadaver specimens of adult shoulders were used. Plain anteroposterior roentgenograms were normal in all of these shoulders. Each cadaver was placed in the supine position and, using image intensification, an 18-gauge needle was inserted immediately anterior to the middle of the distal tip of the acromion and was advanced downward in a vertical direction until the subacromial bursa was entered. Three types of injection into the subTHE JOURNAL OF BONE AND JOINT SURGERY

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steroids). All fifty patients were examined clinically, and acromial bursa were used: fifteen milliliters of air, four teen milliliters of air combined with one milliliter of 30 per plain roentgenograms and glenohumeral arthrograms were cent Renografin radiopaque contrast medium, and fifteen made when they were first seen. In forty-eight of the pa tients arthrography of the glenohumeral joint was followed milliliters of radiopaque latex. Anteroposterior roentgenograms were then made. immediately by subacromial bursography. None of these Most specimens were subsequently frozen and sectioned patients had evidence of instability of the glenohumeral into slabs (0.5 to one centimeter in thickness) in the fron joint, a partial or full-thickness tear of the rotator cuff, or changes demonstrated by clinical examination, tal, transverse, or sagittal plane. Roentgenograms and calcifi photographs of these slabs were then made. Two intact plain roentgenograms, or glenohumeral arthrography. Of specimens were macerated sufficiently to show the rela the fifty patients who originally were included in this tionship of the coracoacromial ligament and the subacro- study, thirty-one could be located and returned for reevaluation. Follow-up ranged from eighteen to sixty-eight mial bursa. months, with an average of 26.4 months. At this reResults evaluation, each patient was interviewed and examined by Of the twenty specimens, four were discarded be one of us. In all but two of the patients, the examination was cause of faulty injections and one was dissected without prior injection. In the remaining fifteen specimens, the performed right after single-contrast glenohumeral ar cap-like subacromial bursa was shown to be situated over thrography. When the shoulder arthrogram demonstrated the rotator cuff (Figs. 1-A through 1-E). Three distinct no rotator-cuff tear (a prerequisite for inclusion in this components of the bursa could be recognized, but not in study), subacromial bursography was performed by the every specimen. These were the subacromial, subdeltoid, technique developed by one of us (T. S.) to establish and subcoracoid portions. The subacromial and subdeltoid whether there was an incomplete tear on the superior sur portions were present and confluent in all specimens ex face of the rotator cuff or whether there was any prolifera cept one, in which a septum separated these two portions. tion or thickening of the synovial membrane or abnormal The subcoracoid portion was demonstrated in only three of ity in the size or shape of the subacromial (or subdeltoid) the specimens. It extended more inferiorly than the rest of bursa. the bursa and lay anterior to the subscapularis tendon. It The patient was placed supine on the fluoroscopy did not communicate with the anterior recess of the table and the skin on the anterior aspect of the shoulder was prepared with Betadine (povidone-iodine). The glenohumeral joint. In the specimen that was dissected without injection, acromion was visualized fluoroscopically in an anteroposthe subacromial bursa extended superiorly under the terior projection and a site for injection was located about acromion and coracoacromial ligament, medially and in two millimeters lateral to the middle of the anterior margin feriorly to the coracoid process, and laterally to the greater of the acromion. Under local anesthesia, a 20-gauge spinal tuberosity. In addition, it extended distally superficial to needle was advanced vertically until its tip contacted the the bicipital groove and under the fibers of the deltoid edge of the acromion. The needle was then displaced muscle for variable distances. Further medially it extended caudally, still maintaining its vertical orientation while it posterior to the coracoid process, between the sub was advanced deeper along the undersurface of the acro scapularis and the coracoid, and deep to the origins of the mion in an anteroposterior direction between the inferior short head of the biceps and the coracobrachialis muscles. surface of the acromion and the superior surface of the At its proximal end, the roof of the bursa was firmly at supraspinatus tendon. As the tip of the needle passed the tached to the undersides of the acromion and the coraco margin of the acromion, a gentle popping sound indicated acromial ligament. that the needle had passed through the coracoacromial lig ament into the subacromial bursa. (In patients with subac Clinical Study romial bursitis, placement of the needle was commonly as Materials and Methods sociated with moderate to severe pain at the site of pene The subacromial impingement syndrome is a very tration of the bursa.) Three or four milliliters of 30 percent specific entity which is characterized by local pain, ten Renografin was injected under fluoroscopic control to fill derness, and a popping sensation in the involved shoulder. the subacromial and subdeltoid extensions of the bursa. Muscle strength and plain roentgenograms are normal. In The shoulder was then slowly abducted twice; vigorous the group of 480 patients with this clinical picture seen movement of the shoulder proved not to be necessary to over a five-year period at the Memorial Hospital Medical distribute the contrast material. When the needle was re Center, Long Beach, California, by two of us (A. M. S. moved while the patient remained supine, anteroposterior and D. W. J.), fifty athletic patients failed to respond to a bursograms were made with the humrus both internal in six-week course of conservative treatment (avoidance of and external rotation. We made a transaxillary bursogram the aggravating activities, application of heat, anti- also only in those patients who had not had shoulder ar inflammatory medication, physical therapy including thrography immediately before the bursogram, because stretching, and at least one subacromial injection of when there is contrast medium in the joint a transaxillary
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FIO.

1-A

FIG. l-B

Figs. I-A through 1-E: Anatomical studies of the subacromial bursa. Fig. 1-A: A normal shoulder with the subacromial bursa injected with radiopaque contrast medium and air. Fig. 1-B: Anterior view of a dissected shoulder, showing the subacromial bursa (arrowhead) filled with latex, the coracoid process (c), the acromion (a), and the coracoacromial ligament (arrow).

bursogram is of no value, as the shadow of the contrast medium in the joint obscures the outline of the bursa. When the bursogram was made in conjunction with the shoulder arthrogram, the thickness of the rotator cuff was

Results The configurations and sizes of the thirty-one sub acromial bursae that were injected varied. Twenty were of

Fio. I-C

FIG. 1-D

Fig. 1-C: Superior view of the injected subacromial bursa (arrowhead), the coracoid process (c), the acromion (a), and the coracoacromial ligament (arrow). Fig. 1-D: Transverse section through the shoulder, showing the coracoid process (c) and the subacromial extension (open arrow) of the subacromial bursa (arrowhead). The biceps tendon (t) and deltoid muscle (d) are also seen.

easily discernible and any defects in the outer surface of the rotator cuff were evident. As we gained experience in placing the needle prop erly, we came to assume that if we were unable to inject the subacromial bursa, the volume of the bursa was too small to accommodate any contrast medium.

normal size (Fig. 2), four were sent. Of the twenty normal-sized cent) had no separation between deltoid portions. In his cadaver communication between these

small, and seven were ab bursae, eighteen (90 per the subacromial and subdissections. Harfound a two portions in 77.9 per

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cent of shoulders. In our series there was no communica tion with the subcoracoid bursa in the twenty shoulders in which the bursa was of normal size, whereas Horwitz and Tocantins found such a communication in 11 per cent of their specimens. Of the eleven abnormal bursae in our series, four ap peared small and abnormally shaped on bursography and seven were not demonstrated. In the seven shoulders in which the orthopaedic radiologist was unable to demon strate a subacromial bursa. the bursa was interpreted as being abnormal. The rotator cuff appeared as a radiolucent band of considerable thickness between the bursa and the glenohumeral joint space when both the bursa and its joint were opacified. In the region of the supraspinatus, the thickness was generally ten millimeters. The outline of the contrast material in the normal bursa was smooth, with no ulcer-like extensions into the underlying cuff. The acromioclavicular joint did not fill with radiopaque material in any patient. The thirty-one patients were categorized according to their clinical response. At the time of follow-up, there were two distinct groups of patients: those who were doing well and those who were still moderately or severely dis abled. The eighteen patients who were doing well had re turned to the activities that originally had been associated with the onset of their shoulder disability. However, some

Fie. 2
Normal subacromial double-contrast bursogram, with the glenohu meral joint also injected with contrast medium. Note the extent of the bursa and the thickness of the cuff.

FIG. l-h
Slab roentgenogram of the specimen shown in Fig. I-D. Note the sub acromial extension (open arrow) of (he subacromial bursa (arrowhead), the coracoid process (c). and the bicipital groove (g).

were competing in the sports activities using a modified technique or on a less rigorous schedule. At the time of writing, none had sought further treatment. The thirteen patients who had moderately or severely limited shoulder function at follow-up were unable to re turn to their previous activities. Most complained of
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chronic shoulder pain, often at rest and at night. The thirty-one patients were also categorized into two groups on the basis of the results of their subacromial bursograms. Group I (twenty patients) had subacromial bur sae that were normal in size, and Group II (eleven patients) had small or absent bursae. The mean ages of the patients were twenty-eight years (range, nineteen to fifty years) in Group I and 34.6 years (range, seventeen to forty-nine years) in Group II. The results of treatment were generally more favorable in the patients in Group II (with abnormal subacromial bursograms) than in those in Group I (with normal bursograms) after an average follow-up of 26.1 months (range, eighteen to sixty months). All of the eleven patients in Group II had subacromial injections of steroids, but only four had a favorable re sponse. Five of the patients who did not improve satisfac torily with non-operative treatment had surgical decom pression of the subacromial arch. In one of these five, op eration and biopsy confirmed non-specific synovitis and a thickened edematous bursa with a normal-appearing rotator cuff. In three others none of the tissue excised at biopsy could be identified histologically as being bursal or synovial. Four of the five patients had only minimum shoulder complaints nineteen to thirty-rive months (mean, 24.4 months) after operation. The fifth patient, whose re sult was classified as a failure after operation, had a thin, degenerated supraspinatus tendon associated with a subac romial osteophyte. but had a normal-appearing subacro mial bursa even though the bui soprani made three months before operation had been abnormal. This patient con tinued to have pain and weakness after exploration and de compression of the coracoacromial arch. Re-exploration nineteen months later showed a full-thickness rupture of the supraspinatus tendon, which was repaired. When he was last seen, ten months after the repair, the pain and

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weakness had decreased considerably but the patient had not been able to return to throwing in competitive sports. The six Group-11 patients who were treated nonoperatively had minimum or no disability when last seen, after an average follow-up of 28.5 months (range, twenty-one to thirty-nine months). The twenty patients in Group I (normal subacromial bursograms) in general had a poor response to treatment, after an average follow-up of 38.6 months (range, thirty to eighty months). Twelve of these twenty patients were un able to engage in athletics. All twenty had subacromial in-

.'
X

excised bursal tissue was available for the third patient who had only mild disability after operation. One year or more after surgical treatment, the other six Group-I patients were still disabled and had been un able to participate in their former sports activities. At follow-up, three of these six patients showed evidence of multiplanar instability of the involved shoulder which had not been apparent during the first few evaluations. Of these three patients, two subsequently underwent repair for anteroinferior instability. Although both had some improve ment of symptoms after repair, they were still moderately disabled when last seen and had been unable to resume ath letic activities with the involved shoulder. The third pa tient with instability refused further surgery and stopped participating in sports involving throwing. In the other three patients who were treated surgically and were still disabled at follow-up, pain was the major complaint, with associated stiffness or so-called clicking in two and with associated weakness in the third. Of the eleven patients in Group 1 who were treated non-operatively and followed for an average of 25.3 months (range, eighteen to sixty-eight months), five had a satisfactory result at the time of follow-up and six had failed to recover sufficiently to resume their previous throwing activities. There was little correlation between the bursographic findings and histological alterations in the bursal tissues in the patients who were operated on (Fig. 3). Of the nine patients with normal bursograms who were treated by surgical exploration and decompression, four showed mild chronic inflammatory changes in the bursa; four showed normal bursal tissue; and one was not evaluated histologically. Only two of the rotator-cuff biopsy specimens from these nine patients demonstrated chronic degenerative changes. The other seven were normal. Discussion

FIG. 3 Histological section of a biopsy specimen of a thinned supraspinatus tendon showing hypocellularity and myxomatous changes (hematoxylin and eosin, x 200).

jection of steroids and only seven had any noticeable im provement. Nine of the twenty had surgical exploration and decompression of the rotator cuff, and after an average follow-up of 28.1 months (range, eighteen to fifty-seven months) only three were improved to the extent that they were almost symptom-free. At operation, two of these three patients showed a thickened coracoacromial ligament with a scarred, fibrotic subacromial bursa, despite their apparently normal preoperative subacromial bursogram. It is noteworthy that both of these patients had satisfactory improvement after surgery. No histolgica! study of the

The clinical examination of the glenohumeral joint, a frequent site of symptoms and signs, is less informative, in many ways, than the examination of other articulations; thus, the accurate diagnosis of subtle glenohumeral insta bility is difficult. Such instability may be clinically appar ent only when the shoulder is overstressed or may cause symptoms only when the joint is subjected to chronic stress in a particularly vulnerable position. Repetitive overuse, as in competitive sports involving throwing, may exaggerate minor degrees of shoulder instability and ini tiate a variety of symptoms and signs. These manifesta tions may not be specific, and differentiation of instability syndromes from coracoacromial arch impingement can be extremely difficult. Compounding this difficulty is the fre quent absence of specific visible signs on plain roentgenograms of patients with glenohumeral joint disability. This insensitivity of routine roentgenography led to the de velopment and refinement of glenohumeral joint arthrography, which may be a valuable diagnostic technique in patients with disruption of the rotator cuff, adhesive capTHE JOURNAL OF BONE AND JOINT SURGERY

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sulitis, or subtle recurrent joint dislocation or subluxation associated with abnormalities of the glenoid labrum. Subacromial bursography has not received much at tention as a diagnostic technique for the evaluation of shoulder abnormalities11. Our results indicate that this procedure may be useful in the management of athletes engaged in sports that involve throwing who complain of subacromial pain. Specific alterations that are visible on a bursogram can provide important information, especially if opacification of the subacromial bursa is combined with prior injection of contrast medium in the glenohumeral joint space. Using these two techniques, the size and configuration of the bursa as well as the thickness and in tegrity of the adjacent rotator-cuff muscles and tendons can be outlined. Bursography makes it possible to identify incomplete or absent filling of the bursa, irregularities in the outline of the bursa (partial tears, adhesions, or syno vial proliferations), and degenerative changes or partial tears on the outer surface of the cuff. Our results suggest that young, symptomatic athletes with normal bursograms who do not respond to conserva tive measures will do poorly following surgical correction of impingement. This finding suggests that some sub acromial pain in athletes engaged in sports involving throwing may not be related to coracoacromial impingement 4,10,15,16 ubtle ligamentous and capsular stretching S due to repetitive overuse of the glenohumeral joint may cause symptoms and signs that are impossible to differ entiate from those related to impingement by the coraco acromial arch and are associated with a normal bursogram.

Under these circumstances surgical procedures to elimi nate impingement will be of no value. This situation ac counted for three of the surgical failures in our patients. On the other hand, the findings in this study also suggest that decompressive procedures can be effective in patients with abnormal bursograms, although they shed no light on the question of how long one should wait before operating on an athlete with an abnormal bursogram and chronic coracoacromial impingement. There is also the question of whether decompression by removal of the coracoacromial ligament predisposes young athletes to rotator-cuff disease or protects them from it. We have fol lowed ten top-level athletes engaged in sports such as men's gymnastics, crew, volleyball, baseball, golf, and tennis for from one to six years after such a release. At the time of writing the patients were nineteen to thirty-se ven years old and had no symptoms or signs to suggest that they may have long-term shoulder disability in the future due to release of the coracoacromial ligament. Whether or not such decompression alters the prognosis of young athletes for rotator-cuff disease remains to be answered12. Subacromial bursography appears to be an additional diagnostic tool for the evaluation of chronic shoulder dis ability. Although we were unable to define subtle distor tions of the outline of the opacified bursae due to osseous or soft-tissue impingement, we believe that with additional experience and use of modern techniques of tomography it should be possible to detect these subtle abnormalities and to improve the accuracy of diagnosis in patients with these disabilities.

References
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