Abstract
Objectives
Unplanned excision (UE) of soft tissue sarcoma (STS) impacts recurrence and prognosis, influenced by various factors. However, few studies have thoroughly analyzed these patients. This study aimed to comprehensively evaluate prognostic factors in patients with STS who underwent UE.
Subject and Methods
We retrospectively identified 62 patients with STS who underwent UE. Data on clinical information and detailed assessment were collected. Clinical data were evaluated as risk factors for overall survival, local recurrence, and distant metastases. Furthermore, associations of influencing factors and survival outcomes were analyzed.
Results
Multivariate analysis identified consultation after local recurrence following previous surgery and histological high grade as significant predictors of poor prognosis (p = 0.0390 and p = 0.0282, respectively). Histological high grade was the only risk factor for distant metastasis (p = 0.0173). Kaplan-Meier curves demonstrated significant differences in overall survival based on the presence or absence of local recurrence at referral after UE (p = 0.0476, p = 0.0022). The use of local anesthetics in previous surgeries was the only risk factor for consultation after local recurrence.
Conclusion
Referral after local recurrence after UE and histological high grade were poor prognostic factors. Physicians must be aware that patients with UE should be referred to specialists promptly.
Keywords: Prognosis, Recurrence, Soft tissue sarcoma, Unplanned excision
Highlights of the Study
This study investigated the prognostic factors in patients with soft tissue sarcoma who underwent unplanned excision.
We included 62 patients with soft tissue sarcoma who underwent unplanned excision, and clinical data were evaluated as risk factors for overall survival, local recurrence, and distant metastases.
Referral after local recurrence after unplanned excision and histological high grade were poor prognostic factors.
Introduction
Treatment of soft tissue sarcoma (STS) generally requires complete removal via wide excision. However, unplanned excision (UE), where tumors are removed without thorough characteristic evaluation, remains a persistent issue in STS treatment. UE often results in R1 or R2 resection margins [1] and insufficient resection, necessitating additional resection. UE is expected to affect local recurrence and prognosis, prompting numerous studies [2–21]. However, opinions vary, with some suggesting that UE does not affect local recurrence or prognosis [2–8], whereas others do not actively recommend additional resection [6, 9, 10].
The impact of UE on recurrence and prognosis is influenced by various factors, e.g., the extent of initial resection, tumor size, use of local anesthetics, timing of patient referral post-resection, and expertise of the specialist managing the case. After referral to a bone and soft tissue tumor specialist, additional factors such as additional resection, radiation, chemotherapy, adjuvant therapy, and residual tumor in resection specimens may also influence outcomes. However, few studies have comprehensively analyzed these factors in patients with UE. Therefore, the present study aimed to examine prognostic factors in detail for patients with STS who underwent UE.
Materials and Methods
Subjects
We retrospectively identified patients with STS with extremity or trunk involvement who underwent UE at a previous hospital and were treated at our two hospitals between 1994 and 2023. Patient records were reviewed to collect data on age, sex, clinical information from the previous hospital (tumor size, magnetic resonance imaging [MRI] use, local anesthetic use, number of surgeries, period from previous surgical resection to consultation, local recurrence, and specialty of previous doctor), tumor size at consultation, anatomical location, histological subtype and malignancy, primary tumor treatment, lung and other metastases, local recurrence, follow-up period, and outcomes. STS specimens were classified using the French Federation of Cancer Center Sarcoma Group system based on the mitotic index, necrosis extension, and histological differentiation [22]. Data on local therapy and surgical margins (Enneking staging system) were collected for patients who underwent surgery [23]. Local recurrence after UE was defined as a palpable mass and local recurrence evident on imaging examinations (e.g., MRI). In the absence of events, patients were deidentified at the last follow-up.
Clinical information was evaluated as risk factors for overall survival, local recurrence, and distant metastases, and the association of these factors with survival outcomes was analyzed. This study was approved by the Institutional Review Board for Clinical Research at Akita University (approval number: 3229) and was conducted in accordance with the Declaration of Helsinki (1975, revised 1983).
Statistical Analyses
All continuous variables are expressed as means ± SD. A Cox proportional hazards model identified factors associated with overall survival, local recurrence, and distant metastases. Multivariate logistic regression analysis identified factors associated with survival outcomes. Kaplan-Meier curves were used for overall survival analysis, with differences assessed using the generalized Wilcoxon test. Statistical significance was set at p < 0.05.
Results
The clinicodemographic characteristics of patients are shown in Table 1. Sixty-two patients (34 males and 28 females) with STS who underwent UE at a previous hospital were included in this study. The mean age was 65.4 years (range: 16–94 years), and the mean tumor size at first visit to the previous hospital was 37.6 ± 24.0 mm (range: 10–150 mm). Twenty-six patients (41.9%) had undergone tumor imaging tests such as ultrasound, computed tomography, or MRI at their previous hospital, of which 20 patients (32.2%) had undergone MRI, the most important imaging method for diagnosing STSs. In 25 patients, local anesthetics had been used in previous surgeries. In 9 patients, multiple UE had been performed at the same hospital; 6 patients had 2, 1 had 4, and 2 had 5 surgeries. The median period from previous surgical resection to consultation was 14.2 ± 36.7 months (range: 1–240 months). In 1 case that took 240 months to be referred to our institutions, UE had been performed 5 times by a previous doctor. Thirty-nine cases were referred to our institutions without obvious local recurrence after UE, and 23 cases were referred after obvious local recurrence was confirmed. The mean tumor size of local recurrence at the time of consultation was 65.5 ± 41.3 mm (range: 16–175 mm). The specialties of previous doctors included orthopedic surgery (n = 25), general surgery (n = 15), plastic surgery (n = 10), dermatology (n = 5), internal medicine (n = 3), neurosurgery (n = 1), otolaryngology (n = 1), cardiovascular surgery (n = 1), and thoracic surgery (n = 1). The primary tumors were present in the lower extremity (n = 22), upper extremity (n = 14), and axial (n = 26). The histological diagnoses of STS were myxofibrosarcoma (n = 17), undifferentiated pleomorphic sarcoma (n = 13), myxoid liposarcoma (n = 10), pleomorphic liposarcoma (n = 3), dedifferentiated liposarcoma (n = 2), malignant peripheral nerve sheath tumor (n = 6), leiomyosarcoma (n = 5), synovial sarcoma (n = 3), extraskeletal myxoid chondrosarcoma (n = 2), and low-grade fibromyxoid sarcoma (n = 1). The French Federation of Cancer Center Sarcoma (FNCLCC) Group classifications were grade I for 14, grade II for 37, and grade III for 11 patients.
Table 1.
Patient characteristics
| | Number (%) |
|---|---|
| Patients | 62 |
| Age | 65.4±18.1 |
| Sex, male/female | 34/28 |
| Size at first visit with previous hospital, mm | 37.6±24.0 |
| MRI before resection at previous hospital | 20 (32.3) |
| Use of local anesthetics in previous surgeries, used/unused/unknown | 25/17/20 |
| Number of surgeries at previous hospitals, one/two/three/four/five | 53/6/0/1/2 |
| Period from previous surgical resection to consultation, months | 14.2±36.7 |
| Consultation after local recurrence following previous surgery | 23 (37.1) |
| Size of local recurrence at the time of consultation, mm | 65.5±41.3 |
| Specialty of previous doctors, orthopedic surgery/other | 25/37 |
| Location, extremity/axial | 36/26 |
| Histological type | |
| Myxofibrosarcoma | 17 (27.4) |
| Undifferentiated pleomorphic sarcoma | 13 (21.0) |
| Myxoid liposarcoma | 10 (16.1) |
| Pleomorphic liposarcoma | 3 (4.8) |
| Dedifferentiated liposarcoma | 2 (3.2) |
| Malignant peripheral nerve sheath tumor | 6 (9.7) |
| Leiomyosarcoma | 5 (8.1) |
| Synovial sarcoma | 3 (4.8) |
| Extraskeletal myxoid chondrosarcoma | 2 (3.2) |
| Low-grade fibromyxoid sarcoma | 1 (1.6) |
| FNCLCC classification, grade I/II/III | 14/37/11 |
| Surgical treatment for primary tumor at our institutions | 55 (88.7) |
| Surgical margin, adequate/inadequate | 50/5 |
| Adjuvant therapy for surgical margin | 9 (16.4) |
| Presence of tumor in resection specimen | 36 (65.5) |
| All chemotherapy | 14 (22.6) |
| Perioperative chemotherapy | 7 |
| All radiotherapy | 8 (12.9) |
| Perioperative radiotherapy | 5 |
| Local recurrence after surgery at our institutions | 10 (18.2) |
| All distant metastases | 19 (30.6) |
| Distant metastasis at the time of presentation to our institutions | 7 (11.3) |
| Follow-up period (months) | 62.2±55.2 |
| Outcome at the last follow-up, NED/AWD/DOD | 44/6/12 |
Values are expressed as numbers of patients or means ± SD with ranges.
FNCLCC, French Federation of Cancer Center Sarcoma Group; NED, no evidence of disease; AWD, alive with disease; DOD, died of original disease; MRI, magnetic resonance imaging.
Additional wide resection after UE or resection for local recurrence after UE for the primary tumors at our institutions was performed in 55 patients (88.7%), and adequate tumor-free margins were achieved in 90.9% (n = 50) of cases. Adjuvant therapy for surgical margins was conducted in 9 patients (16.4%) and included perioperative radiotherapy (n = 5) and acridine orange treatment (n = 4) [24]. The presence of tumor in the resection specimens was confirmed in 36 patients (65.5%). Soft tissue reconstruction after tumor resection included pedicle flaps in 11 cases, free flaps in 5, skin grafts in 11, and amputation in 3 cases. Chemotherapy was administered to 14 patients (22.6%) and included doxorubicin, ifosfamide, dacarbazine, gemcitabine, docetaxel, vincristine, carboplatin, eribulin, trabectedin, and pazopanib. Radiotherapy was performed in 8 patients (12.9%), and radiotherapy plus surgery was performed in 5 patients. Ten patients (18.2%) developed local recurrence. Distant metastases developed in 19 patients (30.6%), of whom 14 developed lung metastases. Extra-pulmonary metastasis sites included lymph nodes (n = 7), bones (n = 3), intraperitoneal (n = 2), soft tissues (n = 1), brain (n = 1), liver (n = 1), and thoracic cavity (n = 1). The mean follow-up period was 62.2 ± 55.2 months (range: 3–316 months). Patient outcomes were as follows: no evidence of disease in 44 patients, 6 were alive with disease, and 12 died from their original disease. No patients died owing to complications during the perioperative period.
Multivariate analysis identified consultation after local recurrence following previous surgery and histological high grade as significant predictors of poor prognosis (p = 0.0390 and p = 0.0282, respectively) (Table 2). Univariate analysis of local recurrence did not identify any significant risk factors (Table 3). However, in a multivariate analysis, histological high grade was the only risk factor for distant metastasis (p = 0.0173) (Table 4). Kaplan-Meier curves showed a significant difference in overall survival between patients with or without local recurrence after UE at the time of referral (p = 0.0476, p = 0.0022) (Fig. 1). Multivariate analysis identified the use of local anesthetics in previous surgeries as the only risk factor influencing consultation after local recurrence following previous surgery, a poor prognostic factor (Table 5).
Table 2.
Univariate and multivariate Cox regression analyses of factors affecting patient prognosis
| Variables | Univariate | Multivariate | ||||
|---|---|---|---|---|---|---|
| OR | 95% CI | p value | OR | 95% CI | p value | |
| Age | 1.035 | 0.991–1.081 | 0.1249 | | | |
| Sex, female | 0.223 | 0.049–1.023 | 0.0535 | | | |
| Size at first visit with previous hospital | 1.020 | 1.001–1.039 | 0.0387 | 1.013 | 0.993–1.034 | 0.1934 |
| MRI before resection at previous hospital | 0.327 | 0.071–1.509 | 0.1518 | | | |
| Use of local anesthetics in previous surgeries | 1.171 | 0.275–4.991 | 0.8313 | | | |
| Multiple resections at previous hospitals | 0.499 | 0.064–3.899 | 0.5074 | | | |
| Period from previous surgical resection to consultation | 0.995 | 0.976–1.015 | 0.6262 | | | |
| Consultation after local recurrence following previous surgery | 5.166 | 1.533–17.405 | 0.0080 | 4.262 | 1.076–16.885 | 0.0390 |
| Specialists other than orthopedic surgeons in previous doctors | 0.890 | 0.280–2.830 | 0.8439 | | | |
| Location, axial | 1.011 | 0.321–3.189 | 0.9849 | | | |
| Histological grade, high | 3.961 | 1.488–10.540 | 0.0058 | 3.625 | 1.112–11.814 | 0.0282 |
| Histological type | ||||||
| Myxofibrosarcoma | 0.797 | 0.215–2.960 | 0.7345 | | | |
| Undifferentiated pleomorphic sarcoma | 0.776 | 0.169–3.564 | 0.7447 | | | |
| All chemotherapy | 4.401 | 1.385–13.981 | 0.0120 | 1.895 | 0.450–7.990 | 0.3839 |
| All radiotherapy | 1.192 | 0.316–4.503 | 0.7952 | | | |
| Surgical treatment for primary tumor | 0.159 | 0.049–0.512 | 0.0021 | 0.282 | 0.067–1.179 | 0.0828 |
| Presence of tumor in resection specimen | 1.118 | 0.204–6.113 | 0.8977 | | | |
| Local recurrence after surgery at our institutions | 0.355 | 0.038–3.316 | 0.3638 | | | |
OR, odds ratio; CI, confidence interval; MRI, magnetic resonance imaging.
Table 3.
Univariate Cox regression analysis of factors affecting the local recurrence of all patients
| Variables | OR | 95% CI | p value |
|---|---|---|---|
| Age | 1.028 | 0.984–1.074 | 0.2199 |
| Sex, female | 0.478 | 0.124–1.850 | 0.2852 |
| Size at first visit with previous hospital | 0.973 | 0.927–1.021 | 0.2604 |
| MRI before resection at previous hospital | 1.328 | 0.375–4.709 | 0.6602 |
| Use of local anesthetics in previous surgeries | 1.449 | 0.292–7.196 | 0.6500 |
| Multiple resections at previous hospitals | 1.608 | 0.339–7.623 | 0.5493 |
| Period from previous surgical resection to consultation | 1.005 | 0.994–1.016 | 0.3986 |
| Consultation after local recurrence following previous surgery | 0.868 | 0.223–3.371 | 0.8375 |
| Specialists other than orthopedic surgeons in previous doctors | 0.661 | 0.191–2.288 | 0.5133 |
| Location, axial | 1.034 | 0.291–3.672 | 0.9587 |
| Histological grade, high | 1.322 | 0.504–3.465 | 0.5708 |
| Histological type | |||
| Myxofibrosarcoma | 1.557 | 0.437–5.551 | 0.4950 |
| Undifferentiated pleomorphic sarcoma | 1.976 | 0.504–7.751 | 0.3289 |
| Surgical margin, inadequate | 2.208 | 0.467–10.430 | 0.3173 |
| Adjuvant therapy for surgical margin | 1.158 | 0.246–5.458 | 0.8530 |
OR, odds ratio; CI, confidence interval; MRI, magnetic resonance imaging.
Table 4.
Univariate and multivariate Cox regression analyses of factors affecting the distant metastasis of all patients
| Variables | Univariate | Multivariate | ||||
|---|---|---|---|---|---|---|
| OR | 95% CI | p value | OR | 95% CU | p value | |
| Age | 1.028 | 0.996–1.060 | 0.0906 | | | |
| Sex, female | 0.665 | 0.261–1.692 | 0.3919 | | | |
| Size at first visit with previous hospital | 1.015 | 1.002–1.028 | 0.0282 | 1.008 | 0.995–1.021 | 0.2097 |
| MRI before resection at previous hospital | 0.876 | 0.332–2.311 | 0.7892 | | | |
| Use of local anesthetics in previous surgeries | 1.006 | 0.328–3.086 | 0.9921 | | | |
| Multiple resections at previous hospitals | 0.319 | 0.043–2.392 | 0.2664 | | | |
| Period from previous surgical resection to consultation | 1.000 | 0.989–1.011 | 0.9977 | | | |
| Consultation after local recurrence following previous surgery | 3.408 | 1.336–8.692 | 0.0102 | 1.965 | 0.703–5.492 | 0.1977 |
| Specialists other than orthopedic surgeons in previous doctors | 0.662 | 0.269–1.632 | 0.3707 | | | |
| Location, axial | 0.565 | 0.214–1.487 | 0.2473 | | | |
| Histological grade, high | 3.215 | 1.511–6.842 | 0.0024 | 2.675 | 1.189–6.016 | 0.0173 |
| Histological type | ||||||
| Myxofibrosarcoma | 0.906 | 0.325–2.528 | 0.8509 | | | |
| Undifferentiated pleomorphic sarcoma | 1.352 | 0.483–3.783 | 0.5658 | | | |
| Presence of tumor in resection specimen | 1.930 | 0.538–6.927 | 0.3131 | | | |
| Local recurrence after surgery at our institutions | 1.005 | 0.279–3.612 | 0.9944 | | | |
OR, odds ratio; CI, confidence interval; MRI, magnetic resonance imaging.
Fig. 1.
Kaplan-Meier curves illustrating overall survival stratified by the presence or absence of local recurrence at the time of referral after unplanned excision (UE). Patients with local recurrence at referral exhibit a significantly poor prognosis (p = 0.0022).
Table 5.
Multivariate analysis of factors affecting consultation after local recurrence following previous surgery
| Variables | OR | 95% CI | p value |
|---|---|---|---|
| Age | 1.014 | 0.960–1.071 | 0.6140 |
| Sex, female | 0.345 | 0.058–2.061 | 0.2433 |
| Size at first visit with previous hospital | 1.048 | 0.996–1.103 | 0.0736 |
| MRI before resection at previous hospital | 0.592 | 0.071–4.913 | 0.6272 |
| Use of local anesthetics in previous surgeries | 10.051 | 1.063–95.017 | 0.0441 |
| Specialists other than orthopedic surgeons in previous doctors | 0.451 | 0.072–2.844 | 0.3968 |
OR, odds ratio; CI, confidence interval; MRI, magnetic resonance imaging.
Discussion
In this study, patients referred after local recurrence following UE had a poor prognosis. However, residual tumor after re-resection and the period between the previous surgery and referral were not cited as factors. Histological high grade was identified as a risk factor for distant metastasis and poor prognosis. As histological high-grade tumors tend to progress more rapidly than low-grade ones, the lack of effect of time to referral on outcome was expected. Unlike our study, prior reports have shown that the presence of tumor in re-resection specimens affects prognosis [9, 11, 12]. The presence of local recurrence in our study suggested that tumor size in additional resected specimens is related to prognosis. UE is often performed by nonspecialists unfamiliar with tumor malignancy or resection margins, highlighting the need to refer patients to bone and soft tissue tumor specialists urgently.
In this study, the only factor influencing referral after local recurrence was the use of local anesthesia during UE. This finding indicates that doctors unfamiliar with tumors who use local anesthesia during removal often delay referral to specialists until recurrence after UE. Among the previous doctors of the participants in this study, orthopedic surgeons were the most common, with specialty differences having no impact on prognosis or patient referral. Education and awareness must be prioritized, especially for orthopedic surgeons, to improve timely referrals.
Imaging, particularly MRI, is crucial in the treatment of STS. Imaging was performed in only 42.1% of patients who underwent UE, with MRIs rarely conducted outside orthopedic departments [13, 14]. In this study, imaging rates were even lower, with only 32.3% of patients undergoing imaging examinations. MRI before UE provides critical information, such as the tail sign, to estimate tumor extent, emphasizing the importance of pre-resection imaging awareness.
A number of previous reports emphasize the need for re-resection in patients with STS after UE [9, 12, 15–20]. However, UE is more likely to be performed in cases of small, shallow, or histological low-grade STS [2, 21], which must be considered when evaluating patients with UE [20]. Additional resection improves local recurrence and prognosis [15–19]. Nakamura et al. [18] conducted a study targeting histological high-grade STS smaller than 5 cm, demonstrating that additional resection improved prognosis. In this study, additional resection was performed in nearly 90% of cases, potentially limiting the evaluation of its effectiveness. Although past studies have highlighted the efficacy of radiation therapy after re-resection [10, 16, 17], the small number of cases involving both radiation therapy and chemotherapy in this study limited its assessment.
This study is the first to comprehensively examine prognostic factors in patients with STS who underwent UE. However, it had some limitations. First, the inability to assess the effect of the histological type of STS could not be evaluated in this study, as the study included 10 different histological STS types, with the most common, myxofibrosarcoma, limited to 17 cases. Myxofibrosarcoma, a histological type prone to local recurrence owing to tissue invasion, highlights the need to consider histological types in future studies. Second was the lack of information on local anesthetic use in some cases, particularly older ones, making it difficult to assess its impact. Although local anesthesia during UE is perceived to affect local recurrence negatively, few studies have investigated this [14]; however, clear evidence is lacking. Therefore, further detailed studies with larger patient cohorts are needed to address these limitations.
Conclusions
This study comprehensively evaluated factors affecting prognosis in patients with STS who underwent UE, identifying referral after local recurrence following UE and histological high grade as poor prognostic factors. In STS treatment, thorough preoperative imaging and biopsy are essential to avoid patient distress. Although UE should be avoided, physicians must be made more aware that, if UE occurs, prompt referral to a bone and soft tissue tumor specialist is essential.
Statement of Ethics
This study was approved by the Institutional Review Board for Clinical Research at Akita University (approval No. 3229) and was conducted in accordance with the Declaration of Helsinki (1975, revised in 1983). All study participants provided informed consent.
Conflict of Interest Statement
The authors have no conflicts of interest to declare.
Funding Sources
The authors have no funding sources.
Author Contributions
Conceptualization and data curation: Hiroyuki Tsuchie and Makoto Emori. Formal analysis, methodology, and writing – original draft: Hiroyuki Tsuchie. Investigations: Hiroyuki Tsuchie, Makoto Emori, Shohei Murata, Yasutaka Murahashi, Emi Mizushima, Junya Shimizu, and Hiroyuki Nagasawa. Project administration: Hiroyuki Tsuchie, Atsushi Teramoto, and Naohisa Miyakoshi. Writing – review and editing: Makoto Emori, Atsushi Teramoto, and Naohisa Miyakoshi.
Funding Statement
The authors have no funding sources.
Data Availability Statement
All data generated or analyzed during this study are included in this article. Further inquiries can be directed to the corresponding author.
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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
All data generated or analyzed during this study are included in this article. Further inquiries can be directed to the corresponding author.