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SECTION I: SYMPOSIUM I: Papers Presented at the 2005 Meeting of the Musculoskeletal Tumor Society

THE CLASSIC: Epiphyseal Chondromatous Giant Cell Tumors of the Upper End of the Humerus

Codman, Ernest Amory

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Clinical Orthopaedics and Related Research: September 2006 - Volume 450 - Issue - p 12-16
doi: 10.1097/01.blo.0000229309.90265.df
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E. A. Codman (1869-1940) was Boston born and bred-Harvard College, Harvard Medical School, and the Massachusetts General Hospital. This is hardly the background one would expect of a medical Don Quixote who spent his life tilting at professional windmills and fighting to advance his ideas, most of which were ahead of his time.

Graduating in the same year that Röntgen discovered X-rays (1895), he was caught up in the enthusiasm surrounding their introduction into medical practice. As early as 1896, he was making routine and contrast X-ray studies of bones and joints. In 1905 he submitted an essay, “The Use of the X-ray in the Diagnosis of Bone Diseases,” for the Gross Prize. It was passed over, the prize being awarded to a paper on the value of carotid artery ligation in the treatment of malignant tumors of the face. From this seminal work came the early X-ray characterization of malignant bone tumors (Codman's triangle), his involvement with the Bone Tumor Registry of the American College of Surgeons and his description of what is now called chondroblastoma of the proximal humerus (Codman's tumor).

As a third-year medical student, he travelled abroad, visiting medical clinics. In Vienna he learned for the first time about the subacromial bursa and its bursitis. His interest piqued, he pursued the subject exhaustively, attracting attention to this condition and eventually publishing a book about the shoulder (Codman's exercises). It is this privately printed book, distributed to his friends, which contains the autobiographical preface revealing the nature and charm of this unusual man.

It was his effort to evaluate the long-term results of surgical treatment, his “End Result Idea,” which engendered the greatest opposition from his colleagues and led to his resignation from the staff of the Massachusetts General Hospital in 1914. His idea was taken up by the Committee on Hospital Standardization and the Society of Clinical Surgery and involved him as a founding member of the American College of Surgeons.

“Perhaps I have sacrificed my success as a distinguished surgeon to these pursuits (hunting and fishing). I have loved them better than teaching dozing medical students, the pride of amphitheatre dexterity, or the hushed dignity of the consultant at the bedside of important persons. On many a bright October day I have been glad that my talents as a teacher were not in demand. In the spring when I dig up the first worm in my garden, I say with Hambone: ‘That old red worm he look up in my face and say, Whar yo’ fishing pole?' Then I get my regard for not being an overworked Chief of the Surgical Service. In summer as I drift about on some out-of-way pond in my portable boat, watching the cotton wool in the clouds, and momentarily expecting a strike from ‘a big one,’ I am grateful I am not in demand at the bankers' bedsides.” (From Codman, E. A., The Shoulder, Boston, T. Todd Co., 1934.)


Giant cell tumors of the upper end of the humerus are either very rare or else they should include the nine tumors in the cases I am about to discuss, which in our series (this study was made from the material collected by the Registry of Bone Sarcoma) have in some instances been called giant cell tumors and in others chondromata, or chondrosarcomata. Evidently a giant cell tumor affects the upper end of the humerus in a different way from that in which it affects the other long bones. Case 117 registered by Bloodgood is the only one which seems to resemble a typical giant cell tumor, and even in this case very little expansion of the bone is shown. There are two other cases, 4 and 556, which are perhaps pure giant cell tumors, but owing to the poor data we have received concerning them, they cannot be seriously considered. I do not know of a single case of typical giant cell tumor in which the growth has expanded the whole upper end of the humerus to the very cartilage of the joint, and which shows the typical trabeculae which are observed in such tumors in other bones. Phemister tells me there is such a specimen at the Presbyterian Hospital in Chicago. It is my belief that the peculiar structure of the head of the humerus makes the picture of giant cell tumor so modified that typical cases do not often occur.

The type of case I allude to in the title is illustrated in the Registry Series by nine tumors of the upper end of the humerus, involving only the portion of the bone in the region of the tuberosities. I wish to call attention to the fact that all the cases in this class are very atypical for either giant cell tumor or osteogenic sarcoma, and that they have a characteristic appearance both by X-ray and in the microscopic slide. It is of interest that the first case (Croxton, Registry 5) has recently been reported by Geschickter and Copeland as a sarcoma.1 On the other hand, Kolodny has reported the same case as a giant cell tumor and illustrates his book with photomicrographs and X-rays from it. The last case in the group, 1031, has been recently reported by Phemister2 as one of chondrosarcoma. Three of the other cases were registered by Coley. Since these men have given serious study to the subject, I cannot lightly take the position that their conclusions have been erroneous, and that in reality, their cases were not malignant but were benign giant cell tumors of this chondromatous type. However, the intermediate seven similar cases in the Registry present such uniformity in the long history prior to operation, the ages of the patients, the good results following conservative treatment, and the unanimity of X-ray and microscopic appearance, that I am personally convinced that all the cases, theirs included, had essentially benign tumors. I believe that this group of tumors is a clinical entity which the surgeon should bear in mind when confronted with tumors of the upper end of the humerus.

In regard to one of these cases (391), of which we have no X-ray, registered by Coley, but which had been operated on in January, 1915, at the University of Michigan, Ewing wrote on the Registry Classification sheet as follows:

Dec. 18, 1923. This appears to be one of the cases of giant cell tumor associated with the absorption of cartilage. Such tumors are generally found at the head of the humerus. The giant cells are rather numerous, typical epulis type, and most numerous about blood spaces. The accompanying cells are peculiar, and are rather large polyhedral granular cells occurring in sheets and clumps. In some areas the giant cells are missing and the polyhedral cells appear exclusively. There are several small foci in which there is dark, staining fibrillar or partly hyaline material, which appears to be degenerating cartilage. There is no sign of bone formation. It does not resemble any of the well known forms of osteogenic sarcoma. Tumor is relatively benign, but probably more active than most giant cell tumors.

The line in italics in which Ewing says, “such tumors are generally found at the head of the humerus,” shows his recognition of this type of tumor. He has also alluded to them in his paper at the 1929 London Congress under the caption of “Calcifying Giant Cell Tumors,” as follows: “I also feel that these tumors are essentially giant cell tumors, and that one must not be deceived by the appearance of chondrosarcoma which they give.”

The much discussed Croxton case, Registry 5, was that of a boy of 16, registered by F. G. Bunts, Cleveland, one of the first cases in the Registry Series. There has been much argument about this case among those interested in the Registry. Bunts consulted Bloodgood and the case appears in Bloodgood's writings as P. N. 26792. Bloodgood favored a preoperative diagnosis of benign tumor but changed this diagnosis to central sarcoma after seeing the specimen. Bunts, however, using his clinical judgment at the operation, decided to treat the case conservatively. He did a very thorough curetting of the tumor and packed with gauze; eight days later he cauterized with zinc chloride, implanted radium, used postoperative X-ray and Coley's toxins. The patient has remained well. Geschickter and Copeland, in their recent article of 1930, still consider the case a sarcoma. In the early days of the Registry, it was considered sarcoma by Ewing, Mallory, Wolbach, Wright, White, Fox, Taylor, and Phemister. Later, Ewing and Bloodgood changed their opinions and agreed with Graham, Stout, Connor, Morton, and the writer, who had considered it a giant cell tumor. It seems to me that in consideration of the other eight cases here presented and the outcome of this case that the diagnosis of giant cell tumor is the correct one. The nine cases may be summarized as follows:

Registry 5. Bunts first saw the case May 1919, five months after the boy had hurt his shoulder while wrestling. During these months, there was a history of the shoulder having slipped out of place and readily slipping back again into the socket. In the last two months there had been much pain, especially at night. There was also scapulohumeral spasm. Bunts first treated the shoulder conservatively with a rubber bandage, but in October 1920, he had X-ray pictures taken which showed the tumor. He then consulted Bloodgood, and operated on October 11, 1920, one year and a half after the first symptoms. The patient was reported to be well ten years later.

Registry 86. Registered by C. C. Simmons, of Boston. A boy of 13 years had had for one year, a hard, smooth tumor, the size of an egg. Curettage was done August 6, 1918. The X-ray picture which was typical of this kind of tumor was poor and was probably taken after curetting. The slide is a good example of this kind of tumor. It presents more giant cell tissue than some of the others. The giant cell tissue verges on the true giant cell tumor type. Patient was well in November, 1922. No further note.

Registry 174. Registered by Coley. No operation was done and hence no slides were made. Patient was a pregnant female, colored, aged 24 years. She was admitted to Memorial Hospital February 1, 1922. She had had pain, with increasing severity, for six months, and a tumor soon followed, July 1921. The method of treatment was not stated. In August 1930, Ewing reported that she was well. The notes were very brief. The X-ray is fairly characteristic of this type of tumor.

Registry 391. Registered by Coley, but had been operated on at the University of Michigan, in January 1915. The patient, a boy of 15 years, had a tumor of the right shoulder. He was unable to raise his arm. Pain had been present for eight months. He gave a history of injury. He was treated afterward with toxins. The slides show the characteristic appearance of these tumors. No X-ray. This is the case on which we quoted Ewing's pathological report. Well in October 1923.

Registry 603. Registered by Coley. Male, aged 15 years, was admitted to hospital February 18, 1924. Six months ago he had pain in the right shoulder, followed by stiffness three months later, with some swelling. He had had electrical treatments with no relief. He was treated with X-ray by Herendeen, and was reported well in January 1927. No slides were made. X-ray films in this case indicate a certain amount of separation of the greater tuberosity, but are fairly characteristic of the group. No history of injury was elicited.

Registry 815. Registered by W. A. Clark of Pasadena, California. A boy aged 20 years, colored, had pain in his arm which began in November 1926. The arm was stiff. He was operated on March 10, 1927, at which time the entire upper end of humerus was resected. He was working in July 1930. The X-ray was very typical, as was the microscopic slide.

Registry 816. Registered by E. T. Dickinson, Greenville, North Carolina. A girl of 17 years, about a year before entering the hospital, noticed a dull pain in the right shoulder. The pain had increased until she could barely use the arm at all. Abduction to more than 20 degrees was impossible. Operation was done October 5, 1926. The tumor was curetted and swabbed with zinc chloride. The supraspinatus and subscapularis were removed and sutured back to the rims of the head. After operation Coley toxins and X-ray treatment were given. She was well, with some limitation of arm movement, in August 1930. X-ray pictures before and after operation were typical of this kind of tumor. The slides were very typical. There was more bone formation than usual. There were areas of giant cells mixed with cartilage and bone.

Registry 902. Registered by H. B. Thomas, Chicago Research Hospital. A girl of 14 years had had pain and difficulty in putting on her coat for a year. She gave no history of trauma. Some swelling was present. She had had some chiropractic treatments. She was operated upon by Hedblom, March 10, 1927, at which time the upper end of the humerus was excised. June 27, 1927, the upper end of the left fibula was transplanted. The wound healed with primary intention. She was well, August 1930, with no sign of recurrence. The slide and the X-ray picture were very typical.

Registry 1031. Registered by D. B. Phemister, in August 1919. Male, aged 22 years. Three and a half years ago, he had slight pain, followed by slight limitation. Operation was done two years ago, by another surgeon; the area of reduced density in the tuberosity being curetted. Symptoms soon recurred, a second curetting was done but no sections were made. Limitation of movement and pain became worse. Phemister resected the upper 6 inches of the humerus, and applied a bone graft in August 1919. The outcome was successful, and the patient was well eight years later. The X-ray is fairly typical of this condition and the slide is very typical. The relative proportion of chondromatous material to giant cells is greater than in the other cases, but this case was operated upon twice before, and had in the meantime passed the age of epiphyseal union.



X-ray characteristics.

These giant cell tumors or chondromata (?) of the upper end of the humerus lie in the angle between the upper and lower epiphyseal lines, i.e., in the greater tuberosity, and are checked at the epiphyseal line of the articular head. Fractures of normal bones in this region are very apt to separate the portions of the bone at the lines of cleavage of the old epiphyses. It appears that in normal bone there is a line of cleavage separating the portion of the bone which is covered with cartilage from the rest of the head, and that this line of cleavage persists long after the epiphyses have united. It may be this line of resistant bone which keeps these tumors from reaching the articular head. At any rate, these tumors do not, as do giant cell tumors in the neighborhood of other joints, actually destroy the bone to the very cartilage. Thus these tumors affect the bone after the manner of osteogenic sarcoma and one always sees in the X-ray picture a small portion of normal bone near the articular surface. This appearance in the lower end of the femur is very characteristic of an osteogenic sarcoma, but it should be discounted when it is found near the head of the humerus. In other words, these peculiar tumors break the rule of giant cell tumors in other bones of progressing through to the very cartilage of the joint, and in the head of the humerus do not extend much beyond the epiphyseal line.

They do not present the characteristic trabeculations which are seen in the X-ray picture of giant cell tumors in other bones. Instead they have a fluffy, “cotton- wool” look. After curettement, they present a fairly characteristic appearance, as if the tumerosities have been gnawed away, thus leaving the articular head and a very definite neck of bone on the inner side. Before curettement, the X-ray examination shows that there is a rather sharp line of demarcation separating the irregular, flocculent mass occupying the region of the greater and lesser tuberosities from the articular head, the inner portion of the neck of the humerus, and the rest of the shaft. A very characteristic feature in all the X-ray films is a buttress of apparently thick, normal, cortical bone on the outer portion of the shaft just below the tumor. This appearance suggests that the tumor has been of quite long duration and nature has supplied reactive bone to strengthen the cortex below it. There is also a thick endosteal layer of bone especially evident in Phe- mister's case 1031, which had been curetted twice before the resection. The outer buttress is not in appearance like the so-called “reactive triangle,” in which there is a triangle between the raised periosteum and the old cortex. It is much more dense and extends much farther down the bone. The buttress is solid and is merely an increase of normal cortical bone, with no invasion of tumor tissue between the old cortex and the periosteum as we seen in osteogenic sarcoma. All nine of these tumors are comparatively small, none being twice as large as the normal head of the humerus.

The microscopic appearances are chiefly distinguished by the presence of peculiar epithelioid cells which merge into a low grade type of cartilage cell on the one hand and into the cells of the tumor on the other. Sometimes the newly formed cartilage forms the bulk of the tumor, and sometimes a tissue indistinguishable from giant cell tumor occupies most of the space. The gross curettings are composed partly of red, friable tissue and partly of whitish, sago-like bits of material or frank cartilage. Sometimes the bulk of one of these tumors is almost wholly cartilage. Perhaps these instances are in slightly older patients, near or just beyond the age of epiphyseal union, e.g., Phemister's case 1031. Sometimes there is a deposit of calcium in the cartilage and new bone formation. It is very likely that some cases may be complicated by infraction and callus.

We frequently find newly formed cartilage and bone toward the periphery of a giant cell tumor, and we sometimes see in giant cell tumors in other parts of the body small areas which correspond to the peculiar tissue seen in these tumors of the humerus. However, we seldom see, in tumors of the other parts, the bulk of the tumor made up by this low grade cartilage and epithelioid cells.

Since we may find similar tissue in true osteogenic sarcomata which involve the epiphyseal lines in this region, it cannot be too strongly stated that the presence of this tissue does not prove that the tumor is benign. I merely wish to make the point that this peculiar tissue probably indicates a benign process and together with the characteristic X-rays and clinical history would justify conservative treatment. In fact, I believe that characteristic X-rays alone are sufficient evidence to justify the institution of radiotherapy without incision. It seems to me that there is reason to believe that if one of these patients were treated with the X-rays alone, the ultimate result would be better. Unfortunately, there are no detailed notes on the end-result of Case 174 which is the only one in which no incision was made.

Clinical points.

The age may prove of importance in diagnosis, when we get a larger series. It is highly probable, as suggested by J. H. Wright, that this cartilage- like tissue is derived from the epiphyseal line. It will be observed that the ages in the cases here presented were in the neighborhood of the time when the epiphyseal lines were still present (given as 12 to 24, but the tumor must have begun earlier in each case). One must bear in mind, too, that the epiphyseal lines in the region of the head of the humerus occupy a relatively larger part of the bone than do such lines in other situations, because there are three separate centers of ossifications: one for each tuberosity, and one for the head. The upper surface of the diaphysis, adjacent to the epiphyseal line, is cone-shaped.

Another clinical point is the relatively long history of symptoms prior to any operation, or the formation of a large tumor, i.e., at the least, six months and an average of over a year. It is of interest to us also that the early symptoms are very similar to those of subacromial bursitis, i.e., pain and restriction of motion. As I have never taken care of one of these patients myself, I cannot speak positively of the early symptoms, and the notes in our cases are very meager, but all mention pain and restriction. However, since these tumors lie just beneath the bursa, it is highly probable that they do produce a bursitis by crowding the enlarged tuberosities under the acromion. There should be a question of this diagnosis in all cases where symptoms of subacromial bursitis occur in persons under 20 years of age, for subacromial bursitis is rare at this time of life and these peculiar tumors occur only at this time of life.

Since all 24 patients with true osteogenic sarcoma of the head of the humerus are dead or very recently registered, a most important clinical point in the 9 cases reported here, is the history of recovery without amputation of the arm. In three of our cases curettements were done; excision was done in one case, resection including the head of the bone was done in three cases. The two others had no operations. Coley's toxins were also used in Registry cases 5, 174, 391, and 816.

Comparative Data of the Nine Cases

I have described these cases in some detail for two reasons. First, because I believe they represent a subordinate clinical entity which should be recognized in the literature, and second, because they are among the few bone tumors which lie in direct contact with a part of the subacromial bursa and give bursal symptoms. In fact, an operator could not thoroughly curette or excise one of them without opening the bursa. If the growth were malignant, one could hardly fail to leave some cells in the bursa. That seven were thus curetted or excised with the bursae opened (and probably also the joint), and extension of the disease did not result, seems strong evidence that the tumors were essentially benign.

Another point is that in our nine cases the clinical judgment of the surgeons in charge was evidently in favor of conservative treatment, for no amputations were done in spite of the pathology.


Since the cases are few in number and the treatment has been outlined in each case, the reader may take his choice of methods. I think I should incline toward mild X-ray therapy, but if I decided to operate, the procedure followed by Dickinson (Registry 816), appeals to me as the best, namely, to excise the tumor and to suture the short rotators to the defect in the head of the humerus. Unfortunately, we have no details about the function of the arm in these nine cases. All are said to have useful limbs, but the degree of usefulness with and without bone grafts cannot be compared without examination of the individual cases.

It is highly probable that similar giant cell tumors may arise in patients between ten and 20 years, in the region of the other skeletal epiphyses, especially in the homologous region of the great trochanter of the femur. I believe that case 277 is such an instance, although in the Registry it is carried as a case of osteogenic sarcoma.

With regard to the name by which to designate this type of tumor. I have used the adjective epiphyseal because I believe that these tumors are characteristic of the period of life when the epiphyses are uniting and that their peculiar cells arise from the epiphyseal cartilage. I have used the adjective chondromatous as descriptive of their histology. I believe that they are essentially benign giant cell tumors and thus that part of their name is justified. Yet I am not satisfied with such a long cumbersome name. Ewing speaks of them as calcifying giant cell tumors, but that does not seem to me descriptive enough. We must find a name which will not tie the tongue but it should associate adolescence with this puzzling type of lesion.


1. Arch. Surg. May 1950, pp. 731-733.
2. Surg. Gynecol. Obstet. 1930, p. 216.
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