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Correspondence   |    
Correspondence
Henrik C. F. Bauer, M.D., Ph.D.; Dempsey Springfield, M.D.; Andrew Rosenberg, M.D.
The Journal of Bone & Joint Surgery.  1997; 79:1591-a-3 
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TO THE EDITOR:
In their Editorial "Biopsy: Complicated and Risky" (78-A: 639—643, May 1996), Springfield and Rosenberg addressed the issue of the biopsy in musculoskeletal oncology. They were disheartened by the results of a study for the Musculoskeletal Tumor Society6 that showed that the conditions of biopsy had not improved compared with those found in a similar study performed eleven years previously5. However, their Editorial lacked an analysis of why things have not improved and also lacked a strategy for change.
Their disappointment was directed toward the medical community, which has not listened to the message of orthopaedic oncologists regarding the value of referring patients who have a bone or soft-tissue tumor to specialized centers before biopsy or marginal excision. This is unfair, and we should instead analyze the message and how it has been conveyed. Changes in referral patterns will be brought about by the education of medical students, residents, and surgeons; by clear recommendations regarding whom and when to refer; and by continuous feedback to the medical community after improper referral. Equally important is positive feedback; a doctor who has referred a patient before a biopsy should be informed of the benefits gained by that specific patient. Feedback should also be provided to all physicians who came into contact with the patient before he or she arrived at the tertiary referral center: family practicians, radiologists, and so on. This concept has proved successful in Sweden, as pioneered by Rydholm10, and more recently in Toronto, as reported by Noria et al.7. Since the indication for biopsy is suspicion of malignancy, open biopsies should never be performed outside of a sarcoma center.
Springfield and Rosenberg were dismayed that the education of residents regarding the hazards of biopsy has had no apparent effect. However, they did not take into account the training that residents receive in the operating room. Residents at the Sloan-Kettering Cancer Center, at the Mayo Clinic, and probably at other sarcoma centers in the United States are allowed to do biopsies. If the message is "do not biopsy," residents should not perform biopsies during their training. Which oncological orthopaedist is obeying the dictum of Mankin4: "The biopsy should be done by a senior and concerned individual who will do the definitive procedure"? The American Board examination for orthopaedic surgeons requires extensive and even cellular knowledge of musculoskeletal neoplasms. This type of detailed, but soon obsolete, knowledge gives young practicing orthopaedic surgeons a false confidence in managing these patients. Instructional Course Lectures in musculoskeletal tumor surgery are given yearly at the meeting of The American Academy of Orthopaedic Surgeons. These provide detailed knowledge for diagnosis and treatment instead of guidelines for referral; hence, an important educational opportunity is missed.
The Scandinavian Sarcoma Group recommends referral to sarcoma centers before biopsy for all patients who have a soft-tissue tumor deep to the fascia, a subcutaneous lesion that is larger than five centimeters, or an osseous lesion that is suggestive of a primary bone neoplasm. The favorable outcome of this policy has been documented repeatedly in the literature1,8,10-13, although Springfield and Rosenberg did not cite these studies in their Editorial. This illustrates a problem in communication not only between the specialists and the medical community but also among the specialists themselves. In Sweden, from 1990 to 1995 the rate of referral before an open biopsy or excision was 71 per cent for patients who had a soft-tissue sarcoma and 88 per cent for those who had an osteosarcoma. Most soft-tissue sarcomas in patients who were referred after an operation were marginally excised subcutaneous lesions; very few were biopsied.
As for the issue of open or closed biopsy, Springfield and Rosenberg were hesitant about but not totally against closed biopsy. I do not agree that a savings of $6000 is negligible14. In fact, if the aforementioned recommendations for referral were followed, only one in ten patients referred for a soft-tissue lesion would be proved to have a malignant tumor; thus, nine of ten would be found to have a benign or reactive lesion by fine-needle aspiration biopsy. Additional workup or treatment is seldom necessary for these patients10. Six thousand dollars is negligible only in the treatment of the few patients who have a high-grade lesion and must receive chemotherapy or radiation therapy, or both, and an extensive limb-salvage procedure.
Fine-needle aspiration biopsy for cytological diagnosis was not discussed at all. This procedure has proved safe and reliable in the diagnosis of both soft-tissue and bone tumors1,3. Although the rate of conclusive diagnoses is lower than that after open biopsy, the rate of incorrect diagnoses is not higher. Furthermore, fine-needle aspiration can be performed before staging studies as a simple outpatient procedure, which saves considerable cost. The cellular material obtained is often sufficient for immunohistochemical staining, flow DNA cytometry, and molecular genetic studies. The use of fine-needle aspiration as a screening method, followed by open biopsy in inconclusive cases, will reduce not only costs but also complications.
Regarding the technique for needle biopsy, I do not agree that it should be performed by an orthopaedic surgeon. Instead, a cytologist or pathologist, who is experienced in the technique, is best suited to obtain optimum cellular material, guided by the orthopaedic surgeon. The point of entry is tattooed for later excision of the biopsy track, although it is not known whether this is necessary after fine-needle biopsy. Computed tomography is seldom necessary to guide the cytologist; fluoroscopy will suffice if it is performed by a radiologist who has been trained in the diagnosis of musculoskeletal tumors. Also, I do not agree that needle biopsy is indicated only for bone lesions with soft-tissue extension. The cortex of intraosseous lesions can, in most cases, be penetrated by the needle, although drilling is necessary occasionally3.
I noted with some surprise their advice regarding subcutaneous soft-tissue tumors. The recommendation that patients who have a benign lesion should be followed appears ill construed since almost everybody has a lipoma. If the decision is made to excise the lesion, inadvertent marginal excision of a small subcutaneous sarcoma is not a catastrophe as long as the deep fascia is not violated. The important message is that a wide excision should not be attempted outside of a sarcoma center.
Finally, continuing efforts to educate the medical community, including feedback to surgeons who refer patients after a biopsy or a marginal excision, will improve referral practices. In Sweden, it has proved more difficult to educate general surgeons, who see many patients who have a soft-tissue tumor, than orthopaedic surgeons, who mostly see patients who have a bone tumor. In the study for the Musculoskeletal Tumor Society, 60 per cent of the patients had a malignant bone tumor6. Since soft-tissue sarcoma is twice as common as bone sarcomas, many patients who have a soft-tissue sarcoma are never referred to a sarcoma center. Hence, the problem in the United States of referral of patients who have a musculoskeletal sarcoma is even larger than Springfield and Rosenberg or Mankin et al.6 believe.
Henrik C. F. Bauer, M.D., Ph.D.: Oncology Service, Department of Orthopedics, Karolinska Hospital, S-171 76 Stockholm, Sweden
Dr. Springfield and Dr. Rosenberg reply:
We are glad that Dr. Bauer shares our concern regarding the difficulties and complications associated with biopsy of musculoskeletal neoplasms. However, he has apparently misinterpreted certain aspects of our Editorial, and while some statements have merit others are inaccurate.
Dr. Bauer states that our Editorial does not include an analysis of why too few patients who have a musculoskeletal neoplasm are referred to specialized treatment centers before a biopsy and that we did not propose a strategy to effect the necessary changes. We disagree and believe that our Editorial addresses these issues in detail. For example, we explained that the philosophical viewpoints taught in medical school, the social circumstances of the patient, the apparent need for the physician to get an immediate answer, and the reluctance of the primary physician to admit that another doctor may be able to offer better care interfere with the recommendation of appropriate referral. Regarding strategy, we emphasized the need for physicians to overcome these barriers and to heed the lessons taught by the scientific studies that were critiqued in our Editorial. We also provided guidelines that help physicians to identify patients who should be referred and presented the proper preoperative planning and operative techniques required to perform the biopsy successfully for physicians who insist on doing the procedure.
Dr. Bauer states that orthopaedic residents should not receive training on how to perform biopsies of musculoskeletal tumors. He also believes that the biological and pathological information that orthopaedic residents are required to know regarding these tumors both is obsolete and leads to "false confidence in managing these patients." Orthopaedic residency training in the United States is based on a different philosophy as it rightly exposes residents to all aspects of the field with the goal of broadening their experience and increasing their understanding of the different disease processes that they encounter. Accordingly, teaching residents how to perform a biopsy or, in the same vein, teaching them any operative procedure that is a part of the specialty is beneficial. However, they should be taught by a knowledgeable and experienced surgeon. This may be a problem in some training programs. Another important part of the resident's education is learning the pathological basis of disease. We believe that considering this type of information obsolete, as Dr. Bauer does, is shortsighted. It is our opinion that a strong education does not breed false confidence in residents and that other, more important factors have produced the problem.
Dr. Bauer correctly points out that the Scandinavian Sarcoma Group has written several articles describing their successful policy regarding the referral of patients who have a soft-tissue tumor1,2,8,10-13. Unfortunately, he admonishes us for not calling attention to this fact in our Editorial, and he believes that we failed to do so because of our lack of familiarity with the orthopaedic literature. Certainly, we are aware of their achievements, as well as those of others, but we did not mention them because our goal was not to present a review of the literature (which should be obvious from our bibliography) but rather to critique three specific articles6,7,14 and offer our point of view on the topic. Therefore, this omission was deliberate.
Dr. Bauer states that we are "hesitant about but not totally against closed biopsy." We do not understand how he derived this impression as we support the use of closed biopsies. We even stated in the Editorial that the article by Skrzynski et al.14 provided an appropriate analysis that forms the "basis for the recommendation of outpatient needle biopsies for properly selected patients." Dr. Bauer strongly suggests that we believe that the money saved ($6000) by performing a closed biopsy instead of an open biopsy for patients who have a musculoskeletal tumor is negligible. This portrayal is inaccurate. We stated that the monetary savings identified by Skrzynski et al. "will not be a substantial percentage of the eventual medical bills of most of these patients" because 71 per cent (forty-four) of the sixty-two patients had some type of malignant musculoskeletal tumor that most likely will lead to prolonged and complicated treatment.
Dr. Bauer believes that the cytologist or pathologist is best suited to perform a needle biopsy. We disagree and believe that any physician member of the treatment team can adequately perform the needle biopsy as long as he or she has received proper training. Dr. Bauer also discusses the utility of fine-needle aspiration, and we agree that it can have an important but selective role in the diagnosis of musculoskeletal tumors. Currently, fine-needle aspiration of musculoskeletal tumors is limited by the rate of accuracy, the lack of guidelines for grading sarcomas with use of tissue obtained with this technique, the inability to perform research because of the small amount of tissue retrieved with this modality, and the fact that many pathologists have little experience with the interpretation of specimens obtained by fine-needle aspiration of these kinds of tumors3,9.
From these discussions, it should be obvious that biopsy of musculoskeletal tumors is complicated and fraught with problems, not only for the patient and the surgeon but also for those who choose to write about it.
Dempsey Springfield, M.D.: Mount Sinai Medical Center, 5 East 98th Street, Box 1188, New York, N.Y. 10029
Andrew Rosenberg, M.D.: Department of Pathology, Massachusetts General Hospital, Fruit Street, Boston, Massachusetts 02114
Åkerman, M.; Rydholm, A.; and Persson, B. M.: Aspiration cytology of soft-tissue tumors. The 10-year experience at an orthopedic oncology center. Acta Orthop. Scandinavica,56: 407-412, 1985.56407  1985 
 
Gustafson, P.; Dreinhöfer, K. E.; and Rydholm, A.: Soft tissue sarcoma should be treated at a tumor center. A comparison of quality of surgery in 375 patients. Acta Orthop. Scandinavica,65: 47-50, 1994.6547  1994 
 
Kreicbergs, A.; Bauer, H. C. F.; Brosjö, O.; Lindholm, J.; Skoog, L.; and Söderlund, V.: Cytological diagnosis of bone tumours. J. Bone and Joint Surg.,78-B(2): 258-263, 1996.78-B(2)258  1996 
 
Mankin, H. J.: Personal communication, 1997. 
 
Mankin, H. J.; Lange, T. A.; and Spanier, S. S.: The hazards of biopsy in patients with malignant primary bone and soft-tissue tumors. J. Bone and Joint Surg.,64-A: 1121-1127, Oct. 1982.64-A1121  1982 
 
Mankin, H. J.; Mankin, C. J.; and Simon, M. A.: The hazards of biopsy, revisited. For the members of the Musculoskeletal Tumor Society. J. Bone and Joint Surg.,78-A: 656-663, May 1996.78-A656  1996 
 
Noria, S.; Davis, A.; Kandel, R.; Levesque, J.; O'Sullivan, B.; Wunder, J.; and Bell, R.: Residual disease following unplanned excision of a soft-tissue sarcoma of an extremity. J. Bone and Joint Surg.,78-A: 650-655, May 1996.78-A650  1996 
 
Rööser, B.; Rydholm, A.; and Alvegård, T. A.: Management of soft tissue sarcoma in Sweden 1982. Acta Orthop. Scandinavica,58: 641-644, 1987.58641  1987 
 
Ryan, M.: Editorial. Cytology and mesenchymal pathology: how far will we go?. Am. J. Clin. Pathol.,106: 561-564, 1996.106561  1996  [PubMed]
 
Rydholm, A.: Management of patients with soft-tissue tumors. Strategy developed at a regional oncology center. Acta Orthop. Scandinavica, Supplementum 203, 1983. 
 
Rydholm, A.: Centralization of sarcoma patients. Acta Oncol.,28 (Supplementum 2): 47-48, 1989.28 (Supplementum 2)47  1989 
 
Rydholm, A.: Soft tissue lesions in adults: biopsy—yes or no?. Ann. Oncol.,31 (Supplementum 2): 57-S58, 1992.31 (Supplementum 2)57  1992 
 
Rydholm, A.; Berg, N. O.; Persson, B. M.; and Åkerman, M.: Treatment of soft-tissue sarcoma should be centralised. Acta Orthop. Scandinavica,54: 333-339, 1983.54333  1983 
 
Skrzynski, M. C.; Biermann, J. S.; Montag, A.; and Simon, M. A.: Diagnostic accuracy and charge-savings of outpatient core needle biopsy of musculoskeletal tumors. J. Bone and Joint Surg.,78-A: 644-649, May 1996.78-A644  1996 
 

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Åkerman, M.; Rydholm, A.; and Persson, B. M.: Aspiration cytology of soft-tissue tumors. The 10-year experience at an orthopedic oncology center. Acta Orthop. Scandinavica,56: 407-412, 1985.56407  1985 
 
Gustafson, P.; Dreinhöfer, K. E.; and Rydholm, A.: Soft tissue sarcoma should be treated at a tumor center. A comparison of quality of surgery in 375 patients. Acta Orthop. Scandinavica,65: 47-50, 1994.6547  1994 
 
Kreicbergs, A.; Bauer, H. C. F.; Brosjö, O.; Lindholm, J.; Skoog, L.; and Söderlund, V.: Cytological diagnosis of bone tumours. J. Bone and Joint Surg.,78-B(2): 258-263, 1996.78-B(2)258  1996 
 
Mankin, H. J.: Personal communication, 1997. 
 
Mankin, H. J.; Lange, T. A.; and Spanier, S. S.: The hazards of biopsy in patients with malignant primary bone and soft-tissue tumors. J. Bone and Joint Surg.,64-A: 1121-1127, Oct. 1982.64-A1121  1982 
 
Mankin, H. J.; Mankin, C. J.; and Simon, M. A.: The hazards of biopsy, revisited. For the members of the Musculoskeletal Tumor Society. J. Bone and Joint Surg.,78-A: 656-663, May 1996.78-A656  1996 
 
Noria, S.; Davis, A.; Kandel, R.; Levesque, J.; O'Sullivan, B.; Wunder, J.; and Bell, R.: Residual disease following unplanned excision of a soft-tissue sarcoma of an extremity. J. Bone and Joint Surg.,78-A: 650-655, May 1996.78-A650  1996 
 
Rööser, B.; Rydholm, A.; and Alvegård, T. A.: Management of soft tissue sarcoma in Sweden 1982. Acta Orthop. Scandinavica,58: 641-644, 1987.58641  1987 
 
Ryan, M.: Editorial. Cytology and mesenchymal pathology: how far will we go?. Am. J. Clin. Pathol.,106: 561-564, 1996.106561  1996  [PubMed]
 
Rydholm, A.: Management of patients with soft-tissue tumors. Strategy developed at a regional oncology center. Acta Orthop. Scandinavica, Supplementum 203, 1983. 
 
Rydholm, A.: Centralization of sarcoma patients. Acta Oncol.,28 (Supplementum 2): 47-48, 1989.28 (Supplementum 2)47  1989 
 
Rydholm, A.: Soft tissue lesions in adults: biopsy—yes or no?. Ann. Oncol.,31 (Supplementum 2): 57-S58, 1992.31 (Supplementum 2)57  1992 
 
Rydholm, A.; Berg, N. O.; Persson, B. M.; and Åkerman, M.: Treatment of soft-tissue sarcoma should be centralised. Acta Orthop. Scandinavica,54: 333-339, 1983.54333  1983 
 
Skrzynski, M. C.; Biermann, J. S.; Montag, A.; and Simon, M. A.: Diagnostic accuracy and charge-savings of outpatient core needle biopsy of musculoskeletal tumors. J. Bone and Joint Surg.,78-A: 644-649, May 1996.78-A644  1996 
 
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