Abstract
In case of sarcomas with intra-articular extension, extra-articular resection (EAR) provides good local control. However, during EAR, the joint capsule may be injured by error, causing tumoral joint fluid leakage, but its impact on oncological outcomes is still unrevealed. We here call these procedures as ‘inadequate EAR’ and retrospectively investigated the impact in 36 osteosarcoma patients. The affected joints included the knee (27 cases), hip (5), shoulder (3), and wrist (1). Responses of preoperative chemotherapy as ‘controlled’ or ‘progressive’ and surgical margins were also assessed. Among the patients, nine (25%) had inadequate EAR. Responses of preoperative chemotherapy were controlled in 23 cases and progressive in 13 cases. Surgical margins were wide in 31 cases and marginal in 5. The 5-year local control rates were 95.5% and 75% for adequate and inadequate EAR, respectively (p = 0.0488). The inadequate EAR group showed a significantly worse response rate of chemotherapy (p = 0.0459) and a trend towards insufficient surgical margins (p = 0.0876). Cox regression analysis indicated that inadequate EAR was associated with a higher hazard ratio (HR) of 6.81 (p = 0.13), whereas the HR for surgical margins was 1.56 (p = 0.74). Poor response to preoperative chemotherapy increases the likelihood of inadequate EAR and may compromise local control.
Keywords: Extra-articular resection, Osteosarcoma, Leakage of joint fluid, Effraction, Surgical margin, Response to chemotherapy
Subject terms: Bone cancer, Sarcoma, Surgical oncology
Introduction
Achieving a pathologically negative margin (R0) is crucial for the surgical management of bone and soft tissue sarcomas. This necessitates wide resection encompassing not only the tumour but also the reactive area1,2.
Extra-articular resection (EAR) is recommended to excise the affected joint entirely when the tumour extends into or is located near the joint. The application of this procedure has been reported for shoulder3–6, hip7–12, and knee joints13–20. Although EAR is associated with a higher frequency of postoperative complications such as infection, haematoma, and poorer postoperative limb function compared to those of intra-articular resection (IAR)16, it has a significant advantage of preserving the affected limb in cases where local control is difficult with IAR7–9,14.
In clinical practice, some EARs are planned but not completed (inadequate EAR) because of joint capsule injuries and leakage of joint fluid13. After aspiration of the joint fluid and immediate repair of the injured capsule, the EAR procedure with a secure surgical margin is continued16 while considering adjuvant treatment for the contaminated surgical field (such as anhydrous ethanol treatment or postoperative irradiation) and replacement of contaminated surgical instruments19. However, the impact of this inadequate EAR on oncological outcomes such as local recurrence and overall survival is still unclear. Only Housset et al. reported such inadequate EARs as ‘effraction’ and their frequency, but they did not assess their impact on local control or overall survival8.
The final surgical margin is known to be strongly associated with local control in EAR7–9,13; however, the association between inadequate EAR and oncological outcomes has not been investigated. In addition to the surgical margin, chemotherapy also affects local control and overall survival in osteosarcoma. Here, we retrospectively evaluated the impact of EAR achievement (adequate or inadequate EAR) on local control and prognosis compared with surgical margin and the effect of preoperative chemotherapy.
Methods
Patients
This study was conducted in accordance with the ethical principles of the Declaration of Helsinki (revised October 2013) and the Clinical Trials Act (announced 14 April 2017, enacted 1 April 2018) of Japan’s Ministry of Health, Labour and Welfare. All patients received verbal and written information and provided informed consent. This study was approved by our Institutional Review Board. Data were treated under an anonymised number. Personal information was consolidated, anonymised and strictly managed. The correspondence list between anonymisation number and clinical data was kept in a locked storage area. Anonymised research data were stored in an isolated computer with password access in a locked clinical data storage room. No personally identifiable information, such as names, will be published in the publication or report of this research.
Of 218 patients with osteosarcoma who underwent limb-sparing surgery between September 1978 and December 2016 at our hospital, 182 underwent IAR and 36 underwent EAR. The affected joints included 27 knees (22 distal femurs and five proximal tibias), five hips (four proximal femurs and one pelvis), three shoulders (proximal humerus), and one wrist (distal radius). Sixty-seven patients underwent amputations during the study period. The reasons for amputation were tumour extension into the vessels or nerve bundles and multiple skip metastases to the ipsilateral leg. There were no amputations due to tumour extension into the joints.
For patients who tolerated chemotherapy, preoperative chemotherapy was administered based on the MAP (Methotrexate, Adriamycin, and Cisplatin) regimen. The indications for EAR at our hospital were (1) direct extension of the tumour to the joint, (2) abnormal or excessive fluid accumulation in the joint, and (3) intra-articular fracture, on image findings immediately prior to resection. In contrast, intra-articular resection (IAR) was performed in cases where the patient had abnormal joint effusion on MRI before treatment, but the effusion normalized with chemotherapy. This strategy was adopted based on the premise that the disappearance of joint fluid indicated successful resolution of the intra-articular tumor component by the chemotherapy.
The efficacy of preoperative chemotherapy was determined using preoperative imaging. Based on a previous report, patients were divided into two groups: controlled—which ranged from partial response (PR) to stable disease (SD)—and progressive—determined as progressive disease (PD) using Response Evaluation Criteria in Solid Tumours (RECIST)21. One patient who had not received preoperative chemotherapy was placed in the progressive group because he was not receiving chemotherapy and, therefore, could not be considered to have responded to chemotherapy.
Preoperative radiotherapy (30 Gy) was given to 16 patients because it was unclear whether EAR could be performed safely and reliably in our early cases. In contrast, postoperative radiation therapy was not performed if the final surgical margin was greater than the marginal margin, regardless of joint effusion leakage. As a result, postoperative radiation was not performed on any of our cases.
We categorized 36 patients who underwent EAR into two groups: those with fluid leakage from the injured joint capsule (inadequate EAR) and those with a completed resection without joint fluid leakage (adequate EAR).
In the event of joint fluid leakage during EAR, the injured capsule was immediately repaired, the contaminated site was cleaned with anhydrous ethanol or distilled water, and the drapes and surgical instruments were replaced.
The resected specimen was classified as intralesional, marginal, or wide according to the evaluation method22.
Study design
Local control and overall survival of 36 patients who underwent EAR were retrospectively examined based on three variables: (1) type of EAR (adequate/inadequate EAR), (2) surgical margin, and (3) response to preoperative chemotherapy. For the analysis of overall survival, only cases without distant metastasis (M0) were included. For the local control analysis, both cases without distant metastasis (M0) and cases with distant metastasis (M1) were included.
Statistical analyses
Statistical analyses were performed using the JMP software (JMP®, Version 12. SAS Institute Inc., Cary, NC), and p-values < 0.05 were considered statistically significant. Between-group comparisons were made using t-tests for continuous variables and Fishers’ exact or Pearson’s χ square tests for categorical variables. The Kaplan–Meier method was used for survival analysis, and the log-rank test was used to compare the two groups. The Cox proportional hazard model was used for multivariate risk comparisons.
Results
Demographic data
The 36 patients with osteosarcoma who underwent EAR comprised 19 men and 17 women. There were six cases of M1 at the initial visit. The mean observation period was 126.6 months (10–360 months). Intraoperative leakage of joint fluid (inadequate EAR) occurred in 9 of 36 patients (25%). All cases underwent limb-sparing surgery without amputation. Details of the adequate-EAR (27 cases) and inadequate EAR (9 cases) groups are shown in Table 1. The nine cases of inadequate EAR included five knee joints (all distal femurs), three hips (all proximal femurs), and one shoulder. Age, sex, location, size, or presence of distant metastases did not differ significantly at the initial visit.
Table 1.
Demographic data of adequate/inadequate EAR cases.
| Inadequate EAR | Adequate EAR | IAR | p-value | ||||
|---|---|---|---|---|---|---|---|
| n | % | n | % | n | % | ||
| Cases | 9 | 27 | 182 | ||||
| Age |
26.1 (12–60) |
24.2 (13–65) |
22.8 (6–81) |
p = 0.48 | |||
| Sex | p = 0.13 | ||||||
| Male | 4 | 44.4% | 15 | 55.6% | 121 | 66.5% | |
| Female | 5 | 55.6% | 12 | 44.4% | 61 | 33.5% | |
| M | p = 0.98 | ||||||
| 0 | 7 | 77.8% | 23 | 85.2% | 152 | 83.5% | |
| 1 | 2 | 22.2% | 4 | 14.8% | 30 | 16.5% | |
| Site | p = 0.65 | ||||||
| Femur | 8 | 88.9% | 18 | 66.7% | 93 | 51.1% | |
| Tibia | 0 | 0% | 5 | 18.5% | 39 | 21.4% | |
| Humerus | 1 | 11.1% | 2 | 7.4% | 15 | 8.2% | |
| Pelvis | 0 | 0% | 1 | 3.7% | 17 | 9.3% | |
| Other | 0 | 0% | 1 | 3.7% | 18 | 9.9% | |
| Size | p = 0.94 | ||||||
| < 8 cm | 7 | 77.8% | 16 | 59.3% | 138 | 63.3% | |
| ≧8 cm | 2 | 22.2% | 11 | 40.7% | 80 | 36.7% | |
IAR, intra-articular resection; EAR, extra-articular resection.
Treatment and oncological outcomes
The treatment and oncological outcomes in the adequate and inadequate EAR groups are shown in Table 2. Preoperative chemotherapy was administered to 35 of the 36 patients, excluding one patient with worsening performance status due to a pathological fracture of the proximal femur. There were no significant differences in chemotherapy or radiotherapy administration between the two groups. Regarding the response rate to preoperative chemotherapy, the efficacy was ‘controlled’ in 74.1% and 33.3% cases in the adequate and inadequate EAR groups, respectively, indicating a better response rate to chemotherapy in the adequate EAR group (p = 0.0459).
Table 2.
Treatment and oncological outcome of the adequate and inadequate EAR groups.
| Inadequate EAR (n = 9) | Adequate EAR (n = 27) | p-value | |||
|---|---|---|---|---|---|
| n | % | n | % | ||
| Margin | p = 0.0876 | ||||
| Wide | 6 | 66.7% | 25 | 92.6% | |
| Marginal | 3 | 33.3% | 2 | 7.4% | |
| Intralesional | 0 | 0 | |||
| Joint | p = 0.229 | ||||
| Knee | 5 | 55.6% | 22 | 81.5% | |
| Hip | 3 | 33.3% | 2 | 7.4% | |
| Shoulder | 1 | 11.1% | 2 | 7.4% | |
| Other | 0 | 1 | 3.7% | ||
| CT | p = 0.25 | ||||
| Yes | 8 | 88.9% | 27 | 100% | |
| No | 1 | 11.1% | 0 | 0% | |
| RT | p = 0.245 | ||||
| Yes | 2 | 22.2% | 14 | 51.9% | |
| No | 7 | 77.8% | 13 | 48.1% | |
| Response to CT | p = 0.0459 | ||||
| Controlled | 3 | 33.3% | 20 | 74.1% | |
| Progressive | 6 | 66.7% | 7 | 25.9% | |
| Local recurrence | p = 0.148 | ||||
| Yes | 2 | 22.2% | 1 | 3.7% | |
| No | 7 | 77.8% | 26 | 96.3% | |
| Overall survival | p = 1.0 | ||||
| Yes | 6 | 66.7% | 18 | 66.7% | |
| No | 3 | 33.3% | 9 | 33.3% | |
EAR, extra-articular resection.
Local recurrence by final surgical margin was as follows: 25 cases with wide margins, including one case of recurrence; two cases of marginal margin without recurrence; and no cases of intralesional margin in the adequate EAR group. In the inadequate-EAR group, there were six cases of wide margins, including one case of recurrence; three cases of marginal margin, including one case of recurrence; and no cases of intralesional margin. There was a trend towards insufficient surgical margins in resected specimens in the inadequate EAR group (p = 0.0876). Fisher’s exact test showed no significant differences in the recurrence rates and overall survival between the two groups.
Impact on local control
Using the Kaplan–Meier method, the 5-year local recurrence-free survival (LRFS) was 95.5% for adequate EAR and 75% LRFS for inadequate EAR, showing a significantly higher recurrence rate in the latter group (P = 0.0488) (Fig. 1).
Fig. 1.
LRFS based on adequate-/inadequate-EAR.
The 5-year LRFS rate based on surgical margin was 92.6% for wide margins and 80% for marginal margins, which was not significantly different between the EAR groups (p = 0.309) (Fig. 2).
Fig. 2.
LRFS based on surgical margin.
The 5-year LRFS based on the response rate to preoperative chemotherapy was 100% for controlled disease and 71.6% for progressive disease, the latter being significantly lower (p = 0.01) (Fig. 3).
Fig. 3.
LRFS based on response to preoperative chemotherapy.
Impact on survival
The 5-year overall survival of patients undergoing adequate/inadequate EAR showed no significant difference (82.6%, adequate EAR; 80%, inadequate EAR; p = 0.85) (Fig. 4).
Fig. 4.
Overall survival based on adequate-/inadequate-EAR.
Similarly, the 5-year overall survival based on surgical margin was not significantly different (80.8%, wide margins; 100%, marginal margins; p = 0.43) (Fig. 5).
Fig. 5.
Overall survival based on surgical margin.
The 5-year overall survival based on response to preoperative chemotherapy was 89.5% for controlled and 67.5% for progressive disease; a trend towards lower survival was observed in the latter group, although the difference was not significant (p = 0.341) (Fig. 6).
Fig. 6.
Overall survival based on response to preoperative chemotherapy.
Multivariate analysis for local control
Response to chemotherapy and surgical margins are also known to be associated with local control. The Cox proportional hazards analysis was performed by adding inadequate/adequate EAR to the surgical margin and preoperative chemotherapy response and only the response to chemotherapy was significantly associated with local control (p = 0.017).
The types of EAR and surgical margins categorised according to their response to chemotherapy are shown in Table 3. In the controlled group, there were only three cases (13%) of inadequate EAR, whereas in the progressive group, there were six cases (46.2%) of inadequate EAR. The prevalence of inadequate EAR was significantly higher in the progressive group (p = 0.0459). In contrast, the surgical margins were not significantly different between the two groups, with three cases (13%) in the control group being marginal, compared to two cases (15.4%) in the progressive disease group (p = 1.0).
Table 3.
Response to chemotherapy based on EAR type and surgical margin.
| Response to preoperative CT | p-value | ||||
|---|---|---|---|---|---|
| Controlled (n = 23) | Progressive (n = 13) | ||||
| EAR | n | % | n | % | p = 0.0459 |
| Adequate | 20 | 87% | 7 | 53.8% | |
| Inadequate | 3 | 13% | 6 | 46.2% | |
| Margin | p = 1.0 | ||||
| Wide | 20 | 87% | 11 | 84.6% | |
| Marginal | 3 | 13% | 2 | 15.4% | |
EAR, extra-articular resection.
Only two variables—surgical margin and type of EAR—can be controlled by the physician out of the three variables mentioned above. Cox regression analysis of these two variables showed that the inadequate-EAR group had a higher hazard ratio (HR) of 6.81 (p = 0.13), whereas the HR of the surgical margin was 1.56 (p = 0.74) (Table 4). Because no local recurrence occurred in this case series with a controlled chemotherapy response, Cox proportional hazards analysis focusing on the controlled group could not be performed.
Table 4.
HR in local control of joint effraction and surgical margins.
| Variables | HR | 95% CI | p-value |
|---|---|---|---|
| Inadequate-EAR | 6.81 | 0.55–156.68 | 0.13 |
| Surgical margin | 1.56 | 0.067–19.51 | 0.74 |
EAR, extra-articular resection.
The 5-year LRFS rate of the 13 patients with a progressive response was 71.6% (Fig. 3). Analysis of the 5-year LRFS in this group according to EAR type showed 83.3% for adequate EAR and 60% for inadequate EAR, with the latter being lower, although not significantly (p = 0.288) (Fig. 7).
Fig. 7.
LRFS based on EAR type in the group in which preoperative chemotherapy was progressive.
Discussion
Extra-articular resection (EAR) provides good local control in locally advanced cases with tumour extension into the joint. Case series including osteosarcoma and other histological types have reported recurrence rates of 21–34% for hip joints7–10,12, 0–29% for knee joints13–19, and 18.2–19% for shoulder joints4–6 after EAR. The overall recurrence rate in our study was comparatively low (8.3%) for both types of EAR. The differences in recurrence rates between reports may be due to inconsistencies in the indications for EAR, surgeon’s skill, adjuvant treatment in the case of effraction, and surgical margins. Joint effusion and haemorrhage are considered to be tumour-reactive areas, even though the presence of tumour cells is uncertain22,23. Therefore, inadequate EAR involving intraoperative joint fluid leakage should be assessed as a potentially dangerous procedure.
Capanna et al. conducted a detailed study to avoid accidental inadequate EAR and warned against partial preservation of the patella and quadriceps muscles and osteotomy above the tibial tuberosity13. They also classified resection margins into three categories—wide, contaminated wide, and marginal—in a series of 14 cases. They reported that two cases were contaminated wide and one was marginal, and all three cases experienced recurrence13. However, this description of ‘contaminated wide’ refers to intraoperative tumour exposure and is not synonymous with leakage of joint effusion due to capsule injury during EAR. Only Housset et al. used the term ‘effraction’ to describe this inadequate EAR and reported its frequency8. They reported on EAR of the hip, including other tumours as well as osteosarcoma, and that unintended effraction occurred in 24.2% of cases, of which one (12.5%) resulted in amputation 3 months postoperatively. However, the cause of amputation and oncological outcomes of the other cases have not been reported. In our study, inadequate EAR occurred in 9 of 36 EAR cases (25%), and recurrence occurred in 2 of the 9 cases (22.2%). Housset et al. also described that 3 of 33 cases (9%) were not R0 (i.e., marginal or intralesional), but the effect of this effraction or surgical margin on subsequent local control or survival has not been analysed. We investigated the impact of effraction on local control, together with surgical margins and response to chemotherapy. Although response to chemotherapy had the greatest impact on local control, the results of the Kaplan–Meier analysis suggested that effraction was also significantly involved in local control. Additionally, the Cox regression analysis with the two variables that can be controlled by the surgeon—effraction and surgical margin—found a higher HR (6.81) for effraction, with an even more significant impact than surgical margin.
In our study, the chemotherapy response was significantly associated with effraction, and the Cox regression analysis of the three variables showed that only chemotherapy response showed a significant difference with respect to local control. Nevertheless, the response rate to chemotherapy is a variable beyond the surgeon control. Surgeons should be aware of the possibility of reduced local control rates (83.3% to 60%) due to the occurrence of effraction if the response to chemotherapy is poor. While performing EAR, it is necessary to pay great attention not only to securing the surgical margin but also to inadequate EAR, which occurs in one-fourth of the cases.
A local control rate of 75% was achieved even with inadequate EAR, indicating that if joint effusion leaks during surgery, the surgeon should not just abort the procedure, but should immediately aspirate and complete the resection with the correct margins. Alternatively, concerns of effraction should be discussed with the patient preoperatively, and a decision should be made on whether to switch to amputation to prioritise local control in the event. To the best of our knowledge, this is the first study to provide specific figures for this purpose.
Limitations
Histological examination of the joint fluid was not performed in any patient. It is possible that the leaked joint fluid may not have had tumour cell contamination in some of the inadequate EAR cases. However, it is clear from previous reports that if the tumour is close to the joint and fluid accumulates, the presence of a tumour should be suspected, unless the fluid disappears after treatment8. Even if joint fluid cytology is performed, a low number of floating cells can give a false-negative result, making it difficult to prove the presence of tumour cells.
In addition, some tests did not show significant differences owing to the small sample size. This may have led to an unavoidable Beta error. However, other studies have also examined a small number of patients, and most have included tumours other than osteosarcoma and soft tissue malignancies in their analyses. This study attempted to be more precise by restricting the analysis to primary osteosarcomas.
There is an association between response to chemotherapy, surgical margin, and effraction, and this confounding factor cannot be statistically resolved. In addition, there was no local recurrence in patients whose response to chemotherapy was controlled, and no subgroup analysis could be performed. However, inadequate EAR was shown to be more strongly associated with local control rate than with the surgical margin.
The cases in this paper were not studied by joint. However, theoretically, the differences between joints would not be significant with regard to the event of effusion leakage associated with inadequate EAR.
Conclusion
The leakage of joint fluid during EAR tends to occur if the response to preoperative chemotherapy is poor. Effraction would affect local control regardless of the width of the surgical margin. However, local control can still be achieved even if effraction occurs, so surgeons should not abandon limb salvage.
Acknowledgements
This work was supported by the JSPS KAKENHI Grant (grant number: JP22K16762).
Author contributions
Y.F. wrote the manuscript. Y.F., S.M., M.S., K.H., S.S., T.T., and K.A. performed the treatment. Y.F., S.M., T.Y., and K.A. analysed and interpreted the patient data. All authors read and approved the final manuscript.
Data availability
The datasets generated and/or analysed during the current study are not publicly available to protect patient personal data but may be available from the corresponding author upon reasonable request.
Declarations
Competing interests
The authors declare no competing interests.
Ethics approval and consent to participate
All patients receive verbal and written information and provide informed consent before enrolment. This study was approved by the institutional review board named medical research ethics committee of Institute of Science Tokyo on July 30, 2022 (approval number: 2022-006) and of Cancer Institute Hospital of JFCR on July 9, 2024 (approval number: 2024-GB-021).
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets generated and/or analysed during the current study are not publicly available to protect patient personal data but may be available from the corresponding author upon reasonable request.