CODMAN´S LECTURE

10th International Congress of Shoulder and Elbow Surgery   

It is a great honor for me to be able to give the Codman Lecture at the 10th International Congress of Shoulder and Elbow Surgery. International shoulder and elbow surgery has always been very important to me, so I feel very privileged and fortunate. It is amazing to see the interest and growth of shoulder and elbow surgery in South America. In the last 15 years, there has been a great period of accomplishment. It is especially important to me to be here to give this lecture because of all my friends and colleagues in South America. Thank you for your years of friendship, and there are certainly too many for me to mention individually. I want to compliment the Brazilian Shoulder and Elbow Society and their organizing committee for running a truly outstanding meeting. Special thanks to Sergio Checchia and Osvandre Lech, chairmen of the Congress for all the hard work and planning that has gone on to make this a perfect meeting.
I chose the subacromial space for my topic today for three reasons. First, it is the anatomical structure in the shoulder that makes this joint unique among other joints. Secondly, through the years it has demonstrated an evolution of scientific research. Third, it allows me the chance to highlight the contributions of the Columbia Shoulder Service through the years. Without considering the glenohumeral joint, there are many anatomical structures that are involved in the pathology of the subacromial space including the acromion, coracoacromial ligament, acromioclavicular joint, rotator cuff, subacromial bursa, biceps tendon, coracoid, and greater tuberosity. All these structures contribute to the pathology of this space. Furthermore in reference to scientific research, there has been great evolution through the years. Initially, researchers studied anatomy and pathology. Then they devised surgical procedures to try to correct the pathology. Then, in the later part of the 20th century, a great deal of work was done in biomechanics and kinematics in this area, and finally most recently research has turned to biochemistry and molecular biology. We will discuss many of these developments in this talk. Through the years the Columbia Shoulder Service has had 4 generations of shoulder surgeons who have made significant contributions to the study of the subacromial space. The first generation was represented by Harrison McLaughlin, the second generation by Charles S. Neer II, the third generation by Louis U. Bigliani, Evan Flatow, and Roger Pollock, and the fourth generation by William N. Levine, Theodore Blaine, Christopher Ahmad, and Catherine Compito.
Early observations in the subacromial space in the late 1800s and early 1900s by Adams, Lane, and Goldthwaithe reflected differences in acromial shape and size. They felt that increased pressure from this difference in shape on the rotator cuff led to inflammatory degeneration of the structures in the subacromial space and therefore resulted in decreased function. These early researchers were convinced that inflammation was one of the primary pathologies. It is interesting because as we shall see, currently we are back to inflammation as a significant etiology in the subacromial space. In the early 1900s, Meyer, an anatomist from Stanford, thought that one of the primary etiologies for pathology in the subacromial space was attrition. He felt that friction against the acromion by the greater tuberosity and rotator cuff led to pathologic changes in the cuff and biceps and eventually to inflammation and arthritis. Codman who coined the term critical zone in the subacromial space felt that the insertion of the supraspinatus tendon was always involved. He felt that there were multiple etiologies and differed from Meyer whose main emphasis was attrition. Codman felt that trauma, calcium, necrosis, and attrition could all be factors that led to pathology in the subacromial space. Lindblom in 1939 felt that there were intrinsic structural variations within the rotator cuff tendons that could lead to tears both superficially and in the deep part of the tendon. He felt that tension varied in different positions and because of the strain put on the rotator cuff in different positions that this led to tears. The shorter deep parts of tendons were more susceptible to tears. Now, consider that nonhomogenous strain can occur from external pressure on the rotator cuff in abduction and lead to tears on the articular surface. Given the fact that the articular surface layers have decreased mechanical strength and decreased blood supply as has been shown by several researchers, this can lead to a combined pathology. Therefore, my hypothesis is that both intrinsic and extrinsic factors can exist at the same time. Multiple etiologies (variables) exist in the subacromial space leading to different pathology. The amount of expression, that is the relative contribution of these factors determine the pathology that occurs. Therefore, we should keep an open mind as it is not one etiology but rather a combination of etiologies which can lead to pathology.
In the early part of the 20th century, surgeons were concerned with treatment of subacromial space, and this usually resulted in removing parts of the acromion. Unfortunately, too much of the acromion or the wrong part were removed with different approaches. This led to complete, radical and lateral acromionectomies which gave inconsistent results and led to a significant deformity. Bernard Diamond from New York City actually wrote a book and advocated complete acromionectomy. His book was called,. ‘The Obstructing Acromion.’ One of the first contributions to the subacromial space from Columbia was by Harrison McLaughlin who felt that a more reasonable operation was the lateral acromionectomy. This was to remove a thin sliver of bone from the entire lateral part of the acromion. In addition, he laid down some principles of rotator cuff surgery which are still present today: Smooth acromial surfaces, tension free apposition of the cuff, and continuity of the cuff mechanism. Following Dr. McLaughlin, it was Dr. Charles S. Neer II who made significant contributions on the pathology of the subacromial space. This included the impingement syndrome, anterior acromioplasty, disadvantages of acromionectomy, and cuff tear arthropathy. Neer felt that the functional arc is forward and that acromial changes, that is increased slope and spurs, occur on the entire anterior aspect of the undersurface. He devised a procedure which revolutionized the treatment of this problem, anterior acromioplasty. His theory was to remove the entire undersurface of the anterior one-third of the acromion and preserve as much deltoid arch as possible. Furthermore, Neer wrote a paper concerning the disadvantages of acromionectomy. He discouraged this procedure because it was deforming and led to poor results in over 30 patients. Neer also described the outlet impingement which involved acromial prominence, AC joint, and also devised an x-ray view. This x-ray view which was developed at Columbia with Dr. Neer is a lateral x-ray in the scapular plane with a 10°caudal tilt. Dr. Osvandre Lech is seen here helping a patient get into proper position for this view.
Starting in the early 1980s, I became interested in the pathology of the subacromial space and studied acromial morphology. We dissected 224 cadaver shoulders over several years in the laboratory with an average age of 76 years with 21% of these patients having rotator cuff tears. We found that rotator cuff tears increased with age, therefore demonstrating that there is an intrinsic etiology to rotator cuff disease. This has been confirmed by many other cadaver studies. We also felt that variations in acromial shape may contribute to tearing of the rotator cuff. To come to these conclusions, we removed all of the acromions from the cadavers, x-rayed them, traced them out on paper and then correlated our results. Initially, we looked at the angles of the different types of acromions but felt that this was too inaccurate and then devised 3 different types of acromions: type I, flat; type II, curved; and type III, hooked. In our study group, 17% were type I, 43% type II, 39% type III. However, seventy percent of the rotator cuff tears occurred in the type III acromion, demonstrating a statistically significantly correlation that more rotator cuff tears occurred with increase in the acromial shape. This work was done with the help of David Morrison. Following this in conjunction with Greg Nicholson, we studied acromions from the Hamann-Todd Osteological Collection from the Cleveland Museum of Natural History. We studied 210 specimens, 420 acromions, and found that spur formation occurred with an increased frequency after 50 years of age. Before 50 years of age the occurrence was 6 % and after 30%. It is interesting to note in these photos of the characteristic place where the spur formation occurred - the entire anterior aspect of the acromion. Furthermore, we also looked at the sizes of the acromions, and it is very interesting to see that acromial thickness in males is only 7.7 mm and 6.7 mm in females. This is far below what we had assumed is the thickness of the acromion. Then in conjunction with Evan Flatow and John Ticker, we studied the acromiohumeral interval as well as the distance between the acromion and the greater tuberosity, and we found that these distances significantly decreased as the arm was elevated. As far as the acromiohumeral interval, it decreased to 5.7 mm at 90 degrees and then went down to 4.8 at 120 degrees. In reference to the acromion to greater tuberosity distance, this was the least at 90 degrees, 5.8 mm. This demonstrated that the height of the subacromial space varies with arm position. Furthermore there is soft tissue sandwiched in between these two bony structures. If we further consider spur formation, we show that this distance is significantly decreased with the spur formation and can lead to impingement. To further study the subacromial space and surface area of the rotator cuff and the acromion, we turn to a technique called stereophotogrammetry. With this technique which uses computerized surface maps, we were able to create contact patterns and proximity relationships in the subacromial space. This was done in conjunction with Dr. Van C. Mow and Dr. Louis Soslowsky in our biomechanics laboratory. What we found was that increased contact occurred with type III acromions, especially at 90 degrees of elevation. As you increase the curvature of the acromion you increase the amount of pressure and contact on the rotator cuff. This technique was also used to determine how much bone should be removed with an acromioplasty. In this slide I approximated that 7-10 mm should be removed. However, if we go back to earlier work that was done Cleveland, the average acromion thickness is only 7.7 mm in men and 6.7 in women. To study this situation, we used stereophotogrammetry again to look at the effect of acromioplasty on contact on the rotator cuff and the greater tuberosity. Contact patterns were greatly improved with bone removal between 2 and 4 mm. Therefore, minimal bone should be removed from the undersurface of the acromion. It is not the quantity of bone removed, but how smooth the surface becomes. Today, the majority of acromioplasties are done arthroscopically with minimal bone removal. To continue our biomechanics research on the acromion and subacromial contact and the foot print, Dr. Christopher Ahmad in our laboratory has done some interesting work with tendon-to-bone interface motion in assessment of rotator cuff tears and normal tendons. He compared the intact rotator cuff to transosseous repairs to suture anchor repairs using a single row and found that there was increased motion with the suture anchor single-row repairs. In addition, he also studied tendon-to-bone intersurface pressure and found that the transosseous repair had increased tendon compression when compared to the point fixation from the single-row technique.
In the 1990s my interest turned to the coracoacromial ligament. Having studied the spur formation, we felt that this ligament probably was the initial structure involved with spur formation and subacromial impingement. We noticed that it inserted on the anterior surface all the way to the lateral part of the acromion and it was a rigid band. Furthermore, we observed that the ligament has two distant bands, an anterolateral band as well as the posteromedial band. Also the ligament inserted 1.8 mm on average on the anterior part of the acromion from medial to lateral. Work done at the University of Michigan by Dr. Soslowsky, who trained with us in Dr. Mow’s laboratory, showed that the geometric properties of this ligament were changed with rotator cuff tears. The lateral band was shorter and had a larger cross section. Also, the structural properties changed with rotator cuff tears as there was a decrease elastic modulus. Interesting work has been done recently at our institution in conjunction with Dr. Theodore Blaine and Dr. Francis Lee in our laboratory. We have shown in specimens taken from the OR that fibrocartilage is found in coracoacromial ligaments with spurs, so therefore there is a change in the ligament that is actively occurring, and this is with spur formation. The ligament is changing with time. I think this correlates well with the work of Hans Uhthoff.. Certainly, the coracoacromial ligament is not a static structure but is dynamic and changes with time.
Renoux has shown that the coracoacromial ligament extends into the subacromial bursa as a Falx, and this has interested us a great deal at Columbia. Once again, in conjunction with Dr. Theodore Blaine, we started to investigate the inflammatory mediators of the subacromial bursa. These include cytokines, prostaglandins, metalloproteases, and growth factors. Through the years, we have received several grants to study this area. One of the initial studies that we did was to take specimens from patients with rotator cuff tears as well as some controlled patients that had instability surgery. What we were able to show was a significant increase in inflammatory mediators in patients with rotator cuff tears. This included the metalloproteases as well as the cytokines and prostaglandins. Furthermore, we were able to identify Stromal Cell Derived factor as an inflammatory mediator in subacromial bursitis. This was done in conjunction with Dr. Yang Soo Kim in 2005. The technique that was used was the Cytokine Receptor Gene Array. Furthermore, in conjunction with Dr. Kim and Dr. Blaine, we were able to show that there was a significant reduction in this inflammatory mediator Stromal Cell Derived Factor after 4 days of treatment of the bursal cells with Cox-2 inhibitors and dexamethasone. Therefore, there is some rationale then for the treatment of bursitis and inflammation with these medications. Finally, what we were able to do in our laboratory was to create a situation where with mechanical strain we induced activation in cytokines in the subacromial bursa and created inflammation. So this then leads us to a model that we have derived with the bursal cell which we have been studying in our laboratory. In this study, we feel that we can stimulate the bursal cells to become inflamed and then measure the amounts of inflammatory mediators that occur and then find ways to be able to inhibit these inflammatory mediators. Certainly this is a most exciting area of study in the future using molecular biology and biochemistry to study the subacromial space.
It appears that we have come full circle with the study of the subacromial space as initial researchers were convinced inflammation was a significant factor and now we have demonstrated in a laboratory that it certainly is. I would just like to close with the thought that research in the shoulder is an ongoing discipline from which we can draw correlations from the past. The picture you see in front of you is from Leonardo DiVinci in his drawings of the muscles of the neck and shoulder. It is a gentleman that is having difficulty raising his arm, and you can see from the pictures that he has significant atrophy of his supraspinatus and infraspinatus muscles and a relative hypertrophy of his deltoid muscle. He is an older individual. So then we fast forward 480 years later, and we look at a drawing and a picture from Dr. Neer’s textbook shoulder reconstruction in 1990. Here we see a gentleman with a rotator cuff tear having difficulty raising his arm much like Leonardi DiVinci’s gentleman with the same type of atrophy of the supraspinatus and infraspinatus and relative hypertrophy of the deltoid muscle. So I think that we can all be good observers of shoulder pathology and try in the future to be able to come up with conclusions that can help us learn more about the shoulder and solve problems. In conclusion then, the key to understanding the subacromial space is embracing rather than excluding different etiologies that lead to pathology. We have to put them into the proper perspective and take advantage of the new technologies available to us. This will only add to our knowledge in the future.

Thank you for this opportunity, Muito Obrigado.

Louis Bigliani, MD