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The Hazards of the Biopsy, Revisited. For the Members of the Musculoskeletal Tumor Society*

HENRY J. MANKIN, M.D., CAROLE J. MANKIN, M.S.L.S and MICHAEL A. SIMON, M.D., BOSTON, MASSACHUSETTS

Investigation performed at Massachusetts General Hospital, Boston.

	Abstract

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In 1982, members of the Musculoskeletal Tumor Society, representing sixteen centers for the treatment of bone and soft-tissue cancer, compiled data regarding the hazards associated with 329 biopsies of primary malignant musculoskeletal sarcomas. The investigation showed troubling rates of errors in diagnosis and technique, which resulted in complications and also adversely affected the care of the patients. These data were quite different when the biopsy had been carried out in a treatment center rather than in a referring institution. On the basis of these observations, the Society made a series of recommendations about the technical aspects of the biopsy and stated that, whenever possible, the procedure should be done in a treatment center rather than in a referring institution. In 1992, the Musculoskeletal Tumor Society decided to perform a similar study to determine whether the rates of complications, errors, and deleterious effects related to biopsy had changed. Twenty-five surgeons from twenty-one institutions submitted the cases of 597 patients. The results were essentially the same as those in the earlier study. The rate of diagnostic error for the total series (in which cases from referring institutions and treatment centers were combined) was 17.8 per cent. There was no significant difference in the rate of patients for whom a problem with the biopsy forced the surgeon to carry out a different and often more complex operation or to use adjunctive irradiation or chemotherapy (19.3 per cent in the current study, compared with 18 per cent in the previous one). There was also no significant difference in the percentage of patients who had a change in the outcome, such as the need for a more complex resection that resulted in disability, loss of function, local recurrence, or death, attributable to problems related to the biopsy (10.1 per cent in the current study, compared with 8.5 per cent in the 1982 study). Eighteen patients in the current study had an unnecessary amputation as a result of the biopsy, compared with fifteen in the previous study. Errors, complications, and changes in the course and outcome were two to twelve times greater (p < 0.001) when the biopsy was done in a referring institution instead of in a treatment center.

	Introduction

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The Musculoskeletal Tumor Society is an organization whose members are principally orthopaedic surgeons involved in the diagnosis and treatment of connective-tissue tumors. In 1982, the Society reported the results of a sixteen-center cooperative study, the goal of which was to assess the diagnostic accuracy of biopsies of connective-tissue tumors and the effect of inaccurate diagnoses or complications of that procedure on the outcome for the patient¹³. That study showed that more than 18 per cent of 329 biopsies performed before January 1, 1979, resulted in inaccurate diagnoses, and 10 per cent of the biopsies were considered to be non-representative or poorly performed. The biopsy resulted in problems with the skin, soft tissue, or bone in 17 per cent of the patients and, according to the treating orthopaedic surgeon, the treatment plan had to be altered for more than 18 per cent. More than 4 per cent of the patients had an amputation that, in the opinion of the treating orthopaedic surgeon, would not have been necessary had the biopsy been done differently, and in 8.5 per cent the biopsy had an adverse effect on the prognosis or outcome. These findings were three to five times more frequent when the biopsy had been performed in a referring institution rather than in a treatment center. On that basis, it was recommended that patients should be referred to a treatment center before a biopsy rather than after it. In the same issue of The Journal of Bone and Joint Surgery, an editorial⁶ and a current concepts review¹⁹ iterated these points and underscored the need for greater care and more attention to be paid to the biopsy and its venue.

The goal in the present study was to re-examine the hazards of biopsies of connective-tissue tumors. We sought to determine if an intervening eleven years had made any difference in the frequency of errors, complications, or alterations in the outcome, as well as whether the advice regarding earlier referral had been heeded and had had any effect on the ultimate fate of the patients who had a malignant tumor of the musculoskeletal system. We also wanted to assess whether our original article had provided an impetus for other groups to look at aspects of the biopsy in a similar way. Since the publication of the original paper, only a small number of additional studies have been performed that have alluded to the technical aspects of biopsies for musculoskeletal disease^{1-5,8,10-12,17,20}; of these studies, only a few have provided data demonstrating the safety or efficacy of the procedure.

	Materials and Methods

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A questionnaire (Table I), similar in design to the one used in our 1982 study, was distributed to the more than sixty members of the Musculoskeletal Tumor Society. We asked each respondent to gather data for approximately twenty-five consecutive, unselected patients who had had a primary malignant sarcoma of the soft tissues or skeleton and had been managed, in the period beginning on January 1, 1990, with a biopsy followed by definitive treatment. In addition to the completed questionnaire, copies of the pathology reports from both the biopsy and the study of the specimen after the definitive operation were required before a patient could be included in the study. Twenty-five surgeons from twenty-one institutions contributed data on a total of 632 patients. Of these patients, 597 fulfilled the criteria for inclusion in the study.

	Results

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We first determined errors in diagnosis and complications in the total series, in which the cases of patients from the referring institutions and the treatment centers were combined.

Errors in Diagnosis
Errors in diagnosis were ascertained by comparison of the diagnosis made on the basis of the biopsy and the definitive diagnosis. A difference was noted for 106 (17.8 per cent) of the 597 patients from both the referring institutions and the treatment centers combined. In our previous study¹³, we defined these errors as major or minor, depending on whether they resulted in a major alteration in the way that the patient was managed at the treatment center. Major errors included the diagnosis of a chondrosarcoma as an osteocartilaginous exostosis, an osteosarcoma as an aneurysmal bone cyst, and a liposarcoma as a benign fibrous histiocytoma. Of the 106 erroneous diagnoses, eighty-one (twenty-nine at treatment centers and fifty-two at referring institutions) were major errors. The accuracy of many of these diagnoses made on biopsy was questioned on the basis of imaging studies or review of the material by the pathologist at the treatment center. Twenty-eight errors caused a major alteration in the treatment protocol (such as the necessity for a wide resection instead of a marginal one or the addition of radiation to the operative field when it would have otherwise been unnecessary). Twelve errors resulted in a change in the course or outcome, such as an additional, more disabling operation; local recurrence; or death. Seven of the twelve errors led to an otherwise unnecessary amputation.

The twenty-five minor errors included the diagnosis of an angiosarcoma as an undifferentiated sarcoma and a high-grade chondrosarcoma as a dedifferentiated chondrosarcoma.

The numbers of both major and minor errors did not differ materially from those reported in our previous study¹³.

Non-Representative Biopsies
Fifty (8.4 per cent) of the 597 patients had a biopsy that was considered to be technically poor or non-representative. Most of these patients needed a second biopsy. In addition, the reporting oncological surgeons were asked to express a judgment as to whether the biopsy had been performed or planned poorly; according to their assessment, 115 (19.3 per cent) of the procedures were in that category.

Complications of the Biopsy
The biopsy resulted in problems with only the skin in thirteen patients (2.2 per cent), with only the bone in three (0.5 per cent), and with only the soft tissue in twenty-two (3.7 per cent) (Table III). Some combination of these operative problems occurred in ninety-five patients (15.9 per cent), the most prevalent such combination being the skin and soft tissue (forty patients). Twenty-two patients needed either irradiation or some change in the irradiation schedule as a result of complications related to the biopsy, and eight patients had an alteration in the chemotherapy protocol. Nineteen patients had severe local complications (including major problems such as local recurrence, the need for a skin graft, and the need for a more extensive resection of bone).

Alterations in Treatment
As indicated by the reporting oncological surgeon, 115 (19.3 per cent) of the 597 patients needed an alteration in treatment because of problems with the biopsy (Table IV). Certain diagnoses seemed to be associated with a higher frequency of such errors; these included osteosarcoma (fourteen of 159 patients), malignant fibrous histiocytoma (thirty-eight of 111 patients), synovial-cell sarcoma (twenty-one of thirty patients), and leiomyosarcoma (five of nine patients). Soft-tissue tumors were more likely to cause difficulties than those arising from bone, and they did so much more frequently when the biopsy had been performed in a referring institution rather than in a treatment center (36.3 compared with 4.1 per cent; p < 0.001). For example, one patient, a twenty-four-year-old man, had had an intralesional excision in the dorsum of the hand; the lesion was diagnosed as a ganglion by an outside pathologist, but subsequent evaluation in the treatment center revealed it to be an extraskeletal myxoid chondrosarcoma, necessitating a second, wider resection. Another patient, a nineteen-year-old woman, had had a biopsy of a lesion of the ischium, which was diagnosed as fibrous dysplasia in the referring institution; however, on review, it was found to be a low-grade osteosarcoma, necessitating a wide resection that included not only the tumor but a poorly placed biopsy track. A common type of error was a transverse biopsy scar on an extremity that necessitated a much more extensive resection and use of free flaps to close the wound over an irradiated bed.

Accuracy of Needle Biopsy
On the basis of the current study, it was also possible to assess the accuracy for eighty-five fine-needle, Trucut (Baxter Health Care, Valencia, California), or Craig-needle biopsies as compared with that for 408 incisional and 104 excisional biopsies (Table VI). Twenty of the needle biopsies were erroneous and an additional fourteen were considered non-representative or technically poor, yielding a 40.0 per cent rate of diagnostic error for this mode of biopsy. In contrast, only 24 per cent of the open biopsies did not provide a correct diagnosis; this difference is significant (p < 0.01, chi-square test). It should be noted that the difficulties with needle biopsy occurred both in treatment centers and in referring institutions and, with the numbers available, we could detect no significant differences between the two groups. Of greater importance is the fact that the rates of altered treatment and altered outcome as a result of needle biopsy were considerably lower than those for open biopsy (p < 0.03 and p < 0.01, respectively; Table VI). Thus, although needle biopsy is not as reliable as open biopsy, the preferred treatment is less often abandoned because of the consequences of a needle biopsy. It is also fair to state that the data are probably skewed because when a poor sample or a diagnostic dilemma occurred as a result of a needle biopsy the patient was sent to a treatment center for additional analysis and treatment.

Comparison of the Data for the Treatment Centers and the Referring Institutions (Table VII)
In every category except amputation, patients who had the biopsy in a treatment center did far better than those who had it in a referring institution. Of the 282 biopsies done in a referring institution, seventy-seven (27.4 per cent) led to an error in diagnosis, thirty-nine (13.9 per cent) were not representative or were technically poor, 102 (36.3 per cent) led to an alteration in the treatment plan, and forty-nine (17.4 per cent) resulted in a change in the course or outcome. The results of the 316 biopsies performed by a member of the Musculoskeletal Tumor Society in a treatment center were greatly superior; thirty-nine (12.3 per cent) led to an error in diagnosis, eleven (3.5 per cent) were non-representative or were technically poor, thirteen (4.1 per cent) led to an alteration in the treatment plan, and eleven (3.5 per cent) resulted in a change in the course or outcome. The differences between the data for the two types of institutions are significant (p < 0.0001), except with regard to the need for an amputation (Table VII).

Comparison with the Results of the Previous Study¹³
Little changed in the eleven years between the time of data collection for the current study and that for the first (1982) study. None of the data in the current study were significantly different, and the outlook regarding the hazards of the biopsy generally appears to be just as bleak as it was previously.

	Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
The data in the current study demonstrate that about 18 per cent of biopsies of musculoskeletal neoplasms result in an error in diagnosis and about 10 per cent are poorly planned and executed or result in a non-representative sample. Of greater concern, fully 9 per cent result in some sort of skin, bone, or soft-tissue complication, and 10 per cent result in an alteration in the course or outcome. These events occur with far greater frequency when the biopsy is performed in a referring institution rather than in a treatment center, and the difference is highly significant (p < 0.0001).

In our earlier study, we were concerned about several possible sources of bias in interpretation of the data. First, we were concerned about whether the selection of patients by the members of the Musculoskeletal Tumor Society who contributed to the study (as compared with those who chose not to participate) indicated a special set of circumstances in their practice that might have resulted in a higher prevalence of biopsy abnormalities. It is interesting to note that the present group differed from the group in the earlier study both in terms of the location and the size of the participating centers. Of the sixteen centers from the first study, only nine contributed the cases of their patients to the current study; the remaining twelve centers in the later study were regionally distinct and were not involved in the first study. The remarkable concordance of results over eleven years, with different surgeons responding from new participating groups, strongly supports the likelihood that the data are relatively unbiased and valid.

The second issue raised in the earlier study was whether the data might be inaccurate because of the manner in which they had been collected. We asked that only patients who had a malignant tumor be included, and we specifically excluded those who had a benign condition that might have been designated as malignant on the biopsy—certainly an almost equally disastrous event. There may be as many of those as there were patients in the current study. Thus, it is likely that the correct number of errors per unit number of biopsies may exceed that reported in the current series.

The third issue is whether we are expressing bias against the referring institutions chiefly because of referral patterns. If only patients who had an obscure diagnosis or those for whom the biopsy was either indeterminate or technically poor were sent to treatment centers, the results would be skewed to indicate that the referring institutions were relatively less capable of carrying out biopsies, while in fact they may only be more cautious. This may be the case, but if so it should be reflected by a difference in the types of cases referred by the institutions compared with those treated primarily in treatment centers. However, the data from both studies demonstrate that the types of tumors for the two groups were essentially identical and, specifically, that the obscure diagnoses were not more frequent in patients from the referring institutions. It is still possible, particularly as discussed in the section on needle biopsy, that the clinicians in the referring institutions referred patients for whom the biopsy was less illuminating than they had anticipated. However, as these patients subsequently had more problems than those with the same diagnosis who had the biopsy in the treatment centers, it appears that the care rendered in the referring institutions was less than optimum.

If the data presented in this study are considered not only as valid but also as corroborative of those obtained in the earlier study¹³, it is possible to summarize the findings as follows.

First, biopsy of bone and soft-tissue tumors is an inherently difficult procedure, with a high rate of complications, some of which can materially change the outcome of the disease. Furthermore, the modern technology (including computerized tomography and magnetic resonance imaging) available in 1989, compared with that available in 1978, did not materially alter these risks, so the fault appears to lie with the disease itself and, perhaps more importantly, with the surgeon. The surgeon's inexperience or inability to deal with the various problems that may arise contribute to the hazards of the procedure. Also, although needle biopsy is much less likely to cause complications in skin, soft tissue, and bone, its accuracy is poor compared with that of open biopsy. Only about 60 per cent (fifty-one) of the eighty-five needle biopsies led to the correct diagnosis as compared with 76 per cent (390) of the 512 incisional biopsies.

A second issue is the venue for the biopsy. There is little doubt, from both of our studies, that for this particular group of diseases the correct diagnosis obtained by a carefully performed and uncomplicated biopsy is essential to the operative treatment and control of the disease. If the biopsy is unsatisfactory, the outcome also is likely to be unsatisfactory and the cost to the patient as well as to society is greatly increased. Hence, if managed-care facilities tend to recommend that biopsies of putative bone and soft-tissue tumors be done locally to save cost, the data reported in the current study should discourage them from this practice. Not only is it dangerous to more than 17 per cent of patients but presumably it results in much greater cost related to additional procedures needed to "rescue" the patient.

In summary, because the data have not changed since our first study, it seems important to restate several of the recommendations from that report¹³.

1. In any biopsy, there should be certainty that an adequate amount of representative tissue has been obtained, and all procedures should be done without trauma and through the smallest possible incision by an experienced surgeon. Although needle biopsy is less likely to result in complications, its accuracy is far less than that possible with open biopsy.

2. If the pathologist cannot make a diagnosis because of unfamiliarity with bone and soft-tissue tumors, he or she should be urged to seek consultation promptly or, possibly, the biopsy should be performed in a center with an experienced orthopaedic pathologist.

3. If the orthopaedist or other practitioner, or the institution, is not equipped to perform accurate diagnostic studies or definitive operative and adjunctive treatment, regardless of the payment plan, then it is in the patient's best interest to be referred to a treatment center before performance of the biopsy.

NOTE: Twenty-five members of the Musculoskeletal Tumor Society contributed the cases of the 597 patients included in this series, from the following treatment centers: Akron General Medical Center, Akron, Ohio; Beaumont Medical Center, Birmingham, Michigan; Case Western Reserve Medical Center, Cleveland, Ohio; Children's Hospital, Boston, Massachusetts; Creighton University St. Joseph's Hospital, Omaha, Nebraska; Istituto Ortopedica Rizzoli, Bologna, Italy; Jackson Memorial Hospital, Miami, Florida; M. D. Anderson Hospital, Houston, Texas; Massachusetts General Hospital, Boston, Massachusetts; The Mayo Clinic, Rochester, Minnesota; Memorial-Sloan-Kettering Cancer Center, New York, N.Y.; Mount Sinai Hospital Center, Toronto, Ontario, Canada; Oregon Health Science University, Portland, Oregon; Orthopaedic Hospital, Los Angeles, California; Roswell Park Memorial Institute, Buffalo, New York; Rush-Presbyterian-St. Luke's Medical Center, Chicago, Illinois; St. Joseph's Hospital, Denver, Colorado; University of California Medical Center, San Francisco, California; University of Chicago, Chicago, Illinois; University of Minnesota Medical Center, Minneapolis, Minnesota; and University of Utah Medical Center, Salt Lake City, Utah.

	Footnotes

 
*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. No funds were received in support of this study.

Orthopaedic Service GR606, Massachusetts General Hospital, Boston, Massachusetts 02114. Please address requests for reprints to Dr. Mankin.

Section of Orthopaedic Surgery and Rehabilitation Medicine, Mail Code 3079, The University of Chicago Hospitals and Clinics, 5841 South Maryland Avenue, Chicago, Illinois 60637.

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