Annals of Surgical Oncology 8:80-87 (2001)
© 2001 Society of Surgical Oncology
Accuracy of Biopsy Techniques for Limb and Limb Girdle Soft Tissue Tumors
Ina Hoeber,
Andrew J. Spillane, FRACS,
Cyril Fisher, MA, MD, FRCPath and
J. Meirion Thomas, MS, MRCP, FRCS
From the Sarcoma Unit (IH, CF, JMT), Royal Marsden Hospital, London, UK; Institute of Pathology (IH), The Johannes Gutenberg University, Mainz, Germany; and Sydney Cancer Center (AJS), Royal Prince Alfred Hospital, Sydney, Australia.
Correspondence: Address correspondence to: J. Meirion Thomas, Sarcoma Unit, Royal Marsden Hospital, Fulham RD, London SW3 6JJ, England; Fax: 0207-808-2673; E-mail: josephmeririon.thomas{at}rmh.nthames.nhs.uk
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ABSTRACT
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BACKGROUND: The biopsy method of choice for soft tissue sarcomas (STS) of the limb and limb girdle is controversial. There have been no randomized controlled trials that compare incision biopsy with Tru-cut biopsy. We present a large series, which includes an analysis of the effectiveness of Tru-cut core biopsy both in a tertiary referral center as well as from many referring hospitals. This is compared with the other methods of biopsy of all soft tissue tumors (STT) referred to this institution.
METHODS: A retrospective review of all patients who were referred to Royal Marsden Hospital NHS Trust (RMH) from 1989 to 1998.
RESULTS: There were 570 patients (576 lesions) identified. Overall Tru-cut biopsy differentiated benign from malignant tumors with a sensitivity of 99.4%, specificity 98.7%, positive predictive value 99.4%, and negative predictive value 98.7% with similar results for RMH and referral hospitals. Tru-cut identified both tumor subtype and grade in approximately 80% of STS. Incision biopsy had similar sensitivity and specificity for differentiating benign from malignant STT as well as subtype of STS but was less accurate for grade assessment. Tumors from patients who were referred after enucleation had a median maximum tumor diameter (MTD) of 4.9 cm, whereas median MTD of tumors diagnosed at referring hospitals by Tru-cut biopsy was 10.6 cm. (P < 0.001).
CONCLUSION: Tru-cut biopsy is highly sensitive and specific in the diagnosis of STT as well as subtyping and grading of STS. It is equally effective as incision biopsy in all these parameters and has a lesser morbidity. The failure to use Tru-cut biopsy is most likely because of the possibility that STS is not suspected in patients with small tumors even when they are deep to the investing fascia.
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INTRODUCTION
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The diagnostic method of choice for soft tissue sarcomas (STS) is controversial. There has been much discussion in the literature on sarcoma about the advantages and disadvantages of Tru-cut biopsy compared to incision biopsy.1–11 Advocates of open incision biopsy claim that Tru-cut core biopsy does not give the histopathologist sufficient tissue to make a confident diagnosis2 especially when the pathologist is inexperienced and that Tru-cut biopsy is unreliable in differentiating subtype and grade.6,7,9 Those who favor Tru-cut biopsy would argue that at the initial point of diagnosis it is debatable whether information on grade and subtype is going to change management in the majority of cases (except in small round cell tumors) and the diagnosis of benign from malignant is by far the most important information to be achieved from the initial biopsy. Advocates of Tru-cut biopsy also point to its simplicity and lack of complications compared with the more invasive methods.1,3,4,8,10
Most specialists in STS would agree that excision biopsy (enucleation) is the least advantageous method of biopsy4,5,9,10,12,13 because microscopic residual disease is reported to remain in up to 50% of cases12–14 and further management is often compromised and complicated. Recently, there has been a suggestion that enucleation followed by two resections may have a survival advantage over cases which had only one definitive operation.15 This could be seen as having major implications for the correct diagnostic strategy for new STS and may be seen as validating enucleation. We believe this conclusion should not be encouraged until the data are further assessed and validated by a randomized controlled trial.
In the past, no reason has been suggested to explain why enucleation4 is performed as the initial management in such a high percentage of patients. It has always been our hypothesis that excision biopsy of STS is performed because the possibility of a STS diagnosis is not considered especially when the lesion is small and alarm bells are not sounded in the surgeon’s or radiologist’s mind. To assess this, patients who had biopsy performed before referral to RMH were analyzed to determine the maximum tumor diameter (MTD) and investigate any correlation between tumor size and biopsy technique employed.
Therefore, this article aims to give an appraisal of the effectiveness of Tru-cut core biopsy in a tertiary referral center as well as the referring hospitals. This is compared to the other methods of diagnosis of all soft tissue tumors (STT) referred to one institution. We also investigate possible reasons why excision biopsy is still used in more than half the cases diagnosed outside specialty centers4 and discuss the problems with recently published evidence that two resections after excision biopsy may have a survival advantage.15
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METHODS
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A retrospective review of all patients with previously untreated limb and limb girdle STT who were referred to Royal Marsden Hospital NHS Trust (RMH) from 1989 to 1998 was performed. Information was collected on the method of diagnosis and final histopathology. Unfortunately, assessment of depth of the tumor in relation to the investing fascia was not collected. All histopathology discussed had been reviewed at the time of referral by one histopathologist with a specialty interest in STS (CF). Patients who were referred after excision biopsy all underwent wide excision of the tumor bed unless there was a clear history of adequate wide resection from the referring surgeon, supported by histopathological evidence of clear margins. An assessment of the incidence of residual disease was made in these cases.
Statistical analysis for diagnostic methods used compared with the trend in MTD was made using the Mann Whitney Test. Significance was set at P < .05 and 95% confidence intervals (CI) are given for the results for incision biopsy because they are based on small numbers.
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RESULTS
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Final Histopathology
Diagnostic information on 570 patients (576 lesions) was available. Of these, 402 lesions were proven to be STS, 159 lesions were benign STT, and 15 were non-STS malignancies. The tumor types are given in Table 1. The 576 lesions were analyzed as two separate groups depending on whether the biopsies were performed at RMH or were referred after biopsy elsewhere ( Table 2).
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Table 2. Distribution of histopathological diagnostic groups in patients referred to RMH with and without prior biopsy-proven diagnosis
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Diagnostic Methods Used
Table 3 shows the diagnostic methods used for STT and STS at RMH and the referring hospitals, respectively. As can be seen in Table 3, 18 lesions were definitively diagnosed on excision biopsy at RMH, 15 were proven to be benign, and the 3 malignant tumors were widely excised.
Tru-cut Biopsy
To assess the accuracy of Tru-cut biopsy in the diagnosis of STT, the histology of the 314 cores (237 lesions available after resection at RMH as well as a further 77 cases performed outside RMH) was compared to the histology of the resected specimens. However, 55 of these cases were excluded from the analysis. The reasons for exclusion are that the STS was treated by radiotherapy and/or chemotherapy only in 21 patients, 13 had a benign STT not resected, 11 were non-STS malignancies, 7 had non-diagnostic core biopsies (technical failure), 2 had neoadjuvant radiotherapy, and 1 was a patient with an unresectable STS. Therefore, the final assessment was made on 259 patients. The combined RMH and referral center accuracy of Tru-cut biopsy in differentiating STS from benign STT and the accuracy of Tru-cut in differentiating subtype and grade of tumors are demonstrated in Table 4. The one false-negative was a well-differentiated liposarcoma diagnosed as a benign lipoma. The one false-positive was an intramuscular lipoma diagnosed as low grade myxofibrosarcoma. Analysis of Tru-Cut biopsies performed at RMH and elsewhere as two separate groups lead to similar results for differentiating STS from benign STT and for differentiating grade and subtype after review of the histopathology at RMH.
Tru-cut biopsy accurately diagnosed all non-STS malignancies that presented initially as soft tissue masses (Table 1). The most common non-STS malignancy was lymphoma (10 out of 15).
Incision Biopsy
To assess the accuracy of incision biopsy in the diagnosis of STT, the histology of the incision biopsy specimens from 8 lesions at RMH and from 48 tumors outside RMH was compared with the histology of the specimen resected. However, from that total of 56 cases (Table 3), 12 were excluded from this analysis because the STT were not resected in 6 patients, 2 were non-STS malignancies, 2 were STS treated by neoadjuvant chemotherapy, 1 patient was treated with neoadjuvant chemoradiotherapy, and 1 was an unresectable STS. Therefore the final assessment was made on 44 patients. The assessment of the ability of incision biopsy to differentiate STS from STT is demonstrated in Table 5. The one false-negative was a well-differentiated liposarcoma diagnosed as a benign lipoma. There were three wound breakdowns identified in the 56 patients (5.4%) who had incision biopsy.
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Table 5. Accuracy of incision biopsy in the diagnosis of STS from benign STT, diagnosis of subtype of STS and subtype of benign STT, and diagnosis of grade of STS
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Mean Tumor Diameter and Biopsy Method
Assessing the patients with STT who had biopsies performed before referral to RMH, we determined the MTD of 162 cases who had excision biopsy and 77 who had Tru-cut biopsy (Table 3). However, 31 of the 162 excision biopsies and 4 of the 77 Tru-cut biopsies were excluded because the MTD could not be ascertained (for excision biopsy this is usually because the tumor had been removed piecemeal!). The median MTD of 131 STT biopsied by excision was 4.9 cm (range 0.5 to 20 cm) in contrast to a median of 10.6 cm (range 2.5 to 30 cm) of 73 STT biopsied by Tru-cut biopsy. The trend in distribution of methods of diagnosis is statistically significant (P < .001) ( Table 6).
Residual Disease After Excision Biopsy
Of the 140 cases of STS diagnosed by excision biopsy before referral to RMH (Table 3), tumor bed resection was performed in 107 patients and residual disease was found in 60 cases (42.9%). There were 47 resection specimens (33.6%) free of tumor. No tumor bed excision was performed in 33 patients (23.6%) after discussion of resection technique with the referring surgeon and histopathological verification of clear margins.
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DISCUSSION
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Soft tissue tumors have a benign to malignant ratio in a hospital population of 100:1 with the majority of lesions representing benign lipomas.16 Tumors deep to the investing fascia are much more frequently malignant and should be assumed to be so until proven otherwise by representative histology. The biopsy method of choice in STT is strongly contested.1,3,4,6–10,15 This article is different from other series on the topic in that it assesses the performance of our specialist unit and contrasts this to the referring hospitals. We have demonstrated the effectiveness of both incision biopsy and Tru-cut biopsy in both settings, hopefully answering some of the major criticisms of the Tru-cut technique which undoubtedly has lower morbidity.1
Tru-cut biopsy can be performed under local anesthesia at the time of initial consultation. The technique has been criticized because the volume of the tumor offered to the pathologist is too small for full histological evaluation.2,6,7,9 However, this series and others3,4,8,10 have shown that Tru-cut biopsy can reliably differentiate benign from malignant STS. In addition, this article shows that in patients with STS, tumor subtype and grade can be accurately predicted in 80% of patients. This work and earlier work from this institution also demonstrates that the histopathological results from Tru-cut biopsy are reliable even if the mass turns out to be a non-STS malignancy.17 The quality of the Tru-cut cores obtained was equal at the RMH to the referring hospitals which suggests that the technique’s successful performance may not be dependent on the volume of the specialist’s experience. It may be possible that in a retrospective study such as this that the referring hospitals did not admit to a failed Tru-cut attempt in their referral; however, we have made every attempt to exclude this possibility by reviewing all histopathology concerning each referral. The argument that non-specialty pathologists can’t reliably diagnose STS on small samples9 is flawed because even small samples can be sent to a second (specialty) pathologist! The false-negative Tru-cuts for malignancy in this series and others8 are due to well-differentiated liposarcoma being misdiagnosed as lipoma. However this distinction can be difficult even with the whole specimen. We often do a Tru-cut biopsy but base management on CT scan findings and tend to be conservative with this subtype of STS with virtually no metastatic potential. We believe that to reflect negative predictive values as low (79%) for Tru-cut biopsy based on this subtype of STS is misleading.8
Incision biopsy has been stated to be the favored option for the diagnosis of STT for reasons of reliability of assessment by inexperienced pathologists as well as for subtyping and grading the tumor preoperatively. Other than being able to be more confident about the need for postoperative radiotherapy, we have found that taken in conjunction with radiological findings, as long as the tumor is accurately determined to be malignant, information on grade has little potential to alter the subsequent steps in management. Similarly, information on subtype is rarely useful preoperatively other than in the case of small round cell tumors which are easily identified on Tru-cut biopsy. When the evidence to support the assertion of better sensitivity and specificity for incision biopsy compared with Tru-cut for determining subtype and grade is investigated, the most frequently quoted studies are flawed in that they either do not have final resection histopathology in all cases,6 they group FNA and Tru-cut together for assessment of "needle biopsy,"7 or they are based on relatively small numbers.6–8 In this large series, which may be biased by our preference for Tru-cut biopsy, we have accumulated similar numbers of cases with incision biopsy to most of the series which are quoted as demonstrating these factors. All those cases that did not have definitive tumor resection for comparison with the Tru-cut and incision biopsy were excluded. In doing this we have found similar sensitivity for both techniques for diagnosing benign from malignant STT, similar accuracy for subtyping, and somewhat surprisingly, the results for grade were slightly worse for incision biopsy. A possible reason for this finding is that the majority of the incision biopsies were performed at referring centers and as explained below, they are often taken from the dome of the tumor which is likely to have the poorest blood supply and most chance of necrosis and unrepresentative sample. Tru-cut biopsy can be taken in a number of directions through the same small stab incision and this may in fact give more reliable sampling for grade according to this data. We believe the incidence of inadequate sample can be lessened by following the simple principle that if it sinks in formalin, the specimen is usually representative, but if it floats, we take more cores.
Despite the recent counter-intuitive evidence which suggests that re-resection of extremity STS improves patient survival by an unexplained mechanism,15 we still believe that excision biopsy is an undesirable and avoidable error in the initial management of patients with STS. Enucleation usually takes place in the plane of the false capsule and it is known from this series and others that after subsequent tumor bed excision, residual disease remains in about half the cases.12–14 Furthermore, the anatomy returns rapidly to near normal after enucleation, and it is difficult to identify the site of the tumor bed on imaging due to the disturbance caused by surgery. Consequently, at tumor bed excision it frequently happens that more unaffected tissue is removed than would have been necessary had wide surgical resection been performed with the tumor in situ. The only way to avoid this error is to raise awareness and to encourage appropriate biopsy of all tumors deep to the deep fascia.
Open incision biopsy and enucleation require at least day-case admission and often a general anesthetic. The disadvantages of enucleation and (occasionally) incision biopsy are that the scar may be inappropriately placed with reference to the incision required for wide surgical clearance. The incision is often done in a cosmetically pleasing transverse skin crease incision which makes it very difficult to make an appropriate longitudinal incision for a wide or compartmental resection. Furthermore, the incision is usually placed over the dome of the tumor where skin vascularity is most likely to be impaired and consequently the incision may fail to heal or become infected.1 Subsequent tumor fungation through the wound from the incision biopsy (or occasionally an enucleation) is unfortunately not a rare occurrence in our experience. One of the consequences of enucleation, and a common source of referral to this institution with recurrent disease, is the situation where patients have been assessed (or assumed) to have clear margins by the treating physicians, and they are not appropriately referred. This may not only result in inadequate surgery, with close margins or microscopic foci of disease remaining, but also may result in failure to receive appropriate adjuvant radiotherapy with its proven advantages for local control in high grade STS.18–20 These events result in higher rates of local failure with the associated psychological stress, increased morbidity from further treatment and there is increasing evidence that local recurrence events have an impact on survival.21
STS are uncommon tumors and it has been our hypothesis that they are inappropriately excised because the diagnosis was not considered. Patients are frequently referred with letters that state that the preoperative diagnosis was intramuscular lipoma. We therefore looked at the MTD of tumors biopsied outside RMH by excision and Tru-cut biopsy. The results demonstrated that the median MTD of excised tumors was 4.9 cm and that of tumors biopsied by core was 10.6 cm. Stated differently, 66.4% of tumors undergoing excision biopsy were smaller than 5 cm and 86.3% of tumors diagnosed by Tru-cut biopsy were > 5 cm. These data suggest it is the smaller STS that are at greatest risk of enucleation and inappropriate management, when it is this group of patients who have the best prognosis.22,23 The larger STT are more often suspected of being malignant and are more often biopsied appropriately. The recent data presented by Lewis et al. support this contention with 60% of the cases that were re-resected being smaller than 5 cm.15 It could be argued that the reason why more tumors were enucleated when they were small was because they were small and superficial. The work of Heslin et al. and Lewis et al. support this argument to some extent.8,15 Superficial tumors were first recognized to have a better prognosis than those deep to the investing fascia by Hajdu.24 More recently, this parameter has been included in the 5th Edition AJCC and UICC Staging Systems.22,25 When the impact of the changes to these staging systems is assessed, only 5% of cases fall into the new AJCC/UICC stages 1B and 2C and therefore in practice do not have a significant impact.26,27 The presentation of an STS with a superficial location rarely alters our preference for biopsy before definitive management.
Fine needle aspiration biopsy (FNAB) has not featured in this discussion because it is generally agreed that there is no place for FNAB in the diagnosis of primary STS.28,29 It can be a useful confirmation of recurrence.
The recently published study by Lewis et al. has major implications for the diagnostic strategy that should be encouraged for STS.15 The authors conclude that there is a survival advantage for re-resection of STS over those cases that have a single definitive operation (which implies a suitable preoperative biopsy in the majority of cases).15 The authors cannot explain their result but believe they have eliminated all the obvious biases in their analysis. However, all the important data have not been presented in their paper and the authors have not discussed some inconsistencies in their data before reaching their conclusions. First, in the AJCC Stage analysis (data not presented, only discussed in the text), the authors state "In all stages there was a trend toward improved survival for the re-resection group, and this was most apparent and statistically significant (P = .005) for stage III (> 5cm, high grade, and deep) disease."15 In a study where there was a heavy weighting toward the small, superficial STS, this appears to state that the only stage group that reached statistical significance is stage III, which may have had the fewest cases. Second, there is a discrepancy between the 2 groups in the study as far as subtype distribution is concerned. This is particularly noticeable for fibrosarcoma where 85% of cases were in the one operation group. Different subtypes of STS behave in a different biological manner and this can influence the validity of the AJCC Staging System in relationship to them.27 Third, the discrepancy in microscopic margin positivity rate between the 2 groups has not been adequately explained. Positive microscopic margins are a predictor for decreased survival in some studies of extremity STS,21 but this variable is not taken into account in the AJCC Staging System.22 There are only three possible explanations for the margin positivity discrepancy: (1) Either the surgeons were different (obviously not), (2) the tumors were different (this could relate to subtype discrepancies), or (3) the sites of the tumors were different with patients with the more difficult sites being inclined to be referred for a specialist’s opinion. Following this logic, one would assume more cases in the one operation group to be very distal, very proximal in the limb or around neurovascular structures; however, these data have not been presented. Some studies have identified extracompartmental site versus compartmental site of STS as an independent prognostic factor for STS.30,31 This concept has been refuted by Gaynor et al. from the multivariate assessment of a retrospective series of 423 patients and has not been assessed further since then.32 Therefore, we conclude that the counter-intuitive conclusions of Lewis et al. have a number of questions which remain unanswered regarding their validity. In the mean time, these conclusions should not be accepted and definitive preoperative biopsy should be the standard of practice until a randomized controlled trial that could eliminate these biases is undertaken.
In conclusion, every mass deep to the deep fascia is a sarcoma until proven otherwise. The possibility of malignancy tends not to be considered when the tumor is small. Tru-cut biopsy at the time of initial consultation will not only differentiate benign from malignant STT, but will also define tumor subtype and grade in a high proportion of patients. Incision biopsy is equally effective in differentiating STS from benign STT and it has the similar ability to identify subtype and grade of STS; however, it has a higher morbidity than Tru-cut biopsy. Therefore, failure to get an adequate sample or adequate information with the initial Tru-cut can be followed by repeat Tru-cut or if there are specific indications by incision biopsy. Even though recent evidence suggests excision biopsy may be associated with an unexplained improvement in survival, there are unexplained sources of bias in the data used to reach this conclusion. Certainly, in terms of functional outcome, the best results are achieved after planned surgical excision with the tumor in situ.
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Acknowledgments
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This article is part of Miss Hoeber’s dissertation "Tru-cut biopsy in the diagnosis of soft tissue tumors: ten year experience in a pathology reference center" under the supervision of C. J. Kirkpatrick, MD, PhD, DSc, FRCPath, Professor and Director of the Institute of Pathology, the Johannes Gutenberg University, Mainz, Germany (1999/2000; in preparation). The authors thank Dr. R. A’Hern for his assistance with the statistical analysis.
Received for publication March 21, 2000.
Accepted for publication August 18, 2000.
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TOP
ABSTRACT
INTRODUCTION
