Orthopedics

Feature Article 

Influence of Prereferral Surgery in Soft Tissue Sarcoma: 10 Years’ Experience in a Single Institution

Maximilian Zacherl, MD; Norbert Kastner, MD; Matthias Glehr, MD; Susanne Scheipl, MD; Gerold Schwantzer, PhD; Horst Koch, MD; Andreas Leithner, MD; Reinhard Windhager, MD

Abstract

Soft tissue sarcomas are a group of rare mesenchymal neoplasms comprising 0.8% of all malignant tumors. Workup should include medical history, physical examination, magnetic resonance imaging, biopsy, and thoracoabdominal computed tomography scan, in that order. Centralized multimodality treatment in a cross-disciplinary setting is mandatory. Treatment not according to current clinical practice guidelines is a common problem before referral to a specialized institution. The purpose of this 10-year, single-institution review was to investigate the influence of curative surgery on outcome, with a special emphasis on surgery before referral.

A cohort of 266 patients who underwent curative surgery for soft tissue sarcoma between 1998 and 2008 was analyzed. One hundred thirty-one (49%) patients underwent surgery contrary to current clinical guidelines before referral, most (73%) at primary care units. One hundred thirteen (86%) of these patients underwent surgery without previous biopsy with a higher rate of intralesional margins (P<.001), a smaller mean diameter of primary lesion (P<.001), a higher rate of subcutaneous situs (P<.001), a lower mean American Joint Committee on Cancer score (P=.008), a higher rate of additional plastic surgery after re-resection (eg, flap surgery) (P<.001), and a longer period before referral (P<.001). No influence on survival, local recurrence, or metastasis existed.

Prereferral surgery necessitating re-resection has no influence on survival but leads to an unfavorable clinical course. More effort should be made to improve awareness and referral modalities for general practitioners and physicians at community hospitals.

Drs Zacherl, Kastner, Glehr, Scheipl, and Leithner are from the Department of Orthopaedic Surgery, Dr Schwantzer is from the Institute of Medical Informatics, Statistics and Documentation, and Dr Koch is from the Department of Surgery, Medical University of Graz, Graz, and Dr Windhager is from the Department of Orthopaedic Surgery, Medical University of Vienna, Vienna, Austria.

Drs Zacherl, Kastner, Glehr, Scheipl, Schwantzer, Koch, Leithner, and Windhager have no relevant financial relationships to disclose.

Correspondence should be addressed to: Maximilian Zacherl, MD, Department of Orthopaedic Surgery, Medical University of Graz, Auenbruggerplatz 5, 8010, Graz, Austria (max_zacherl@hotmail.com).

Abstract

Soft tissue sarcomas are a group of rare mesenchymal neoplasms comprising 0.8% of all malignant tumors. Workup should include medical history, physical examination, magnetic resonance imaging, biopsy, and thoracoabdominal computed tomography scan, in that order. Centralized multimodality treatment in a cross-disciplinary setting is mandatory. Treatment not according to current clinical practice guidelines is a common problem before referral to a specialized institution. The purpose of this 10-year, single-institution review was to investigate the influence of curative surgery on outcome, with a special emphasis on surgery before referral.

A cohort of 266 patients who underwent curative surgery for soft tissue sarcoma between 1998 and 2008 was analyzed. One hundred thirty-one (49%) patients underwent surgery contrary to current clinical guidelines before referral, most (73%) at primary care units. One hundred thirteen (86%) of these patients underwent surgery without previous biopsy with a higher rate of intralesional margins (P<.001), a smaller mean diameter of primary lesion (P<.001), a higher rate of subcutaneous situs (P<.001), a lower mean American Joint Committee on Cancer score (P=.008), a higher rate of additional plastic surgery after re-resection (eg, flap surgery) (P<.001), and a longer period before referral (P<.001). No influence on survival, local recurrence, or metastasis existed.

Prereferral surgery necessitating re-resection has no influence on survival but leads to an unfavorable clinical course. More effort should be made to improve awareness and referral modalities for general practitioners and physicians at community hospitals.

Drs Zacherl, Kastner, Glehr, Scheipl, and Leithner are from the Department of Orthopaedic Surgery, Dr Schwantzer is from the Institute of Medical Informatics, Statistics and Documentation, and Dr Koch is from the Department of Surgery, Medical University of Graz, Graz, and Dr Windhager is from the Department of Orthopaedic Surgery, Medical University of Vienna, Vienna, Austria.

Drs Zacherl, Kastner, Glehr, Scheipl, Schwantzer, Koch, Leithner, and Windhager have no relevant financial relationships to disclose.

Correspondence should be addressed to: Maximilian Zacherl, MD, Department of Orthopaedic Surgery, Medical University of Graz, Auenbruggerplatz 5, 8010, Graz, Austria (max_zacherl@hotmail.com).

Soft tissue sarcomas are a group of rare mesenchymal neoplasms, comprising 0.8% of all malignant tumors.1 Workup should include medical history, physical examination, magnetic resonance imaging (MRI), biopsy, and thoracoabdominal computed tomography scan, in that order. Basic curative treatment consists of surgery with mandatory wide resection margins, radiation therapy, and chemotherapy.2,3

The incidence of soft tissue sarcomas in Austria for the study period (1998–2008) is approximately 2000 total cases.4 The catchment area of the authors’ institution covers one-third of the population of Austria, approximating an incidence of 660 patients in 10 years. Treatment in tertiary referral centers with multidisciplinary teams, including orthopedic surgeons, oncologists, radiologists, radiooncologists, and pathologists, is mandatory for proper clinical management.5 Current guidelines recommend referral to a tumor center for patients with a soft tissue mass with 1 of the following clinical features: 5 cm or more in size; below the superficial investing fascia; pain or rapid increase in size.2,5,6

Despite these guidelines, the rate of surgical treatment without wide margins is approximately 50% before referral to the authors’ institution. Almost every institution treating patients with soft tissue sarcomas is confronted with this problem.3,6–12 After reexcision with wide resection margins, survival and recurrence rates, as well as incidence of metastases, are similar to those after initial surgery with wide resection margins.7,13,14 One study focused on negative side effects (eg, more mutilating surgery, higher local recurrence rates, and obscure prognosis) from reoperations after previous inadequate surgery.13

The current authors undertook a 10-year data analysis (1998–2008) of patients with soft tissue sarcomas who received curative surgical treatment at their institution to detect the clinical effect of inadequate surgical intervention before curative resection.

Materials and Methods

The study period covered March 1998 to August 2008. The authors’ institution represents a tertiary referral center for bone and soft tissue tumors. Since 1988, all relevant data about patients with tumors of the bone and soft tissue have been entered prospectively in a database. Data of patients with the diagnosis of soft tissue tumor of the extremities and trunk who underwent curative resection were selected with a filter. Clinical follow-up was completed by contacting patients or, if necessary, relatives, general practitioners, and other attending physicians; if all failed, survival was updated by information retrieval from the civil registry office.

During the study period, 296 patients with soft tissue sarcoma were referred to the authors’ institution. Two hundred sixty-six patients underwent curative resection and were included in the study. The men:women ratio was 1.2:1. Median age at resection was 61 years (range, 11–96 years). The most frequent sarcoma location was the thigh and gluteal region (48%), followed by the upper arm (15%), lower leg (14%), forearm (11%), abdominal wall (9%), foot (2%), and hand (2%). Mean size of the primary lesion as measured before initial surgery in 208 patients was 10.2 cm (range, 1–47 cm). The largest dimension was 5 cm or more in 168 (63%) patients. The location of the primary lesion was deep or below the superficial fascia in 180 (70%) patients and subcutaneous in 76 (30%) patients. Mean American Joint Committee on Cancer (AJCC)15 score was 1.96.

One hundred twelve (42%) patients were referred to the authors’ institution without prior surgery. Table 1 shows the institutions where all patients underwent primary surgery. The time from the first onset of symptoms (eg, swelling, pain, and neurological symptoms) to referral to the authors’ institution was obtained from the patient’s history. Surgical intervention before referral was classified as biopsy or intralesional, marginal, or wide resection. The study data do not show that any patient referred to the authors’ institution during the study period underwent previous surgery with wide resection margins. The AJCC score was obtained at the time of admission for curative surgery. Survival status was recorded as survival with no evidence of disease, survival with local recurrence and/or metastasis, death due to disease, and death due to another cause.

Site of Initial Surgical Interventiona

Table 1: Site of Initial Surgical Intervention

The patients were divided into 2 groups: group A comprised patients who were surgically treated according to guidelines and underwent 1 therapeutic surgery at the authors’ institution, and group B comprised patients who were referred to the authors’ institution and underwent re-resection after previous inadequate surgical treatment.

Histopathology

All histological specimens were reviewed by a group of pathologists at the authors’ institution with expertise in the diagnosis of soft tissue sarcoma. Histopathology conformed to current nomenclature according to the World Health Organization classification. If necessary, an international reference pathologist was consulted for an opinion; this was the case with 32 patients. The surgical margin was defined as microscopically positive if the pathologist found tumor at the inked margin of the specimen. Tumor size was defined as the maximum dimension of a freshly resected specimen. In cases of re-resection, the largest dimension according to presurgical imaging was recorded.

Histological grading was high (G3) in 53% of patients, intermediate (G2) in 22% of patients, and low (G1) in 24% of patients. The 3 most frequent histological diagnoses were liposarcoma (25.2%), undifferentiated pleomorphic sarcoma (including the entity formerly known as malignant fibrous histiocytoma16) (20.3%), and leiomyosarcoma (15.0%) (Table 2).

Histology of Study Population

Table 2: Histology of Study Population

Surgical Treatment

The surgical treatment decision was based on histopathology, size, and anatomical location of the primary tumor. The aim of surgery was wide (microscopically negative) resection. In cases of adjacent neuronal structures, function-sparing resection was favored to amputation or mutilating surgery. Seventeen (5.7%) patients required primary amputation. Means of defect reconstruction after curative surgery by plastic surgery were recorded. Type of resection was classified according to Enneking et al.17 Surgical complications were classified according to Goslings and Gouma.18 Additional multiagent chemotherapy and radiotherapy was recorded. External beam radiation with doses of approximately 60 Gy was predominantly applied in high-grade lesions. Indication for adjuvant therapy was given at the discretion of a multidisciplinary institutional tumor board.

The time from the first medical consultation to presentation at the authors’ institution ranged from 0 years, if the patient prsented to the authors’ institution first, to 15 years (mean, 42 weeks; median, 5.5 weeks). Resection margins after definitive surgery at the authors’ institution were intralesional in 1 (0.4%) patient who refused amputation, marginal in 18 (6.6%) patients (including 13 low-grade liposarcomas or lipoma-like liposarcomas), and wide (more than 2 cm healthy tissue) in 247 (93%) patients. Nine patients underwent compartimental (radical) resection. Seventeen amputations and 3 rotational plasties according to Borggreve19 were performed.

Direct wound closure after curative resection was feasible in 152 (57%) patients. Sixty-three (24%) patients underwent flap surgery for wound closure after resection. Twenty-eight (10%) patients were treated with mesh graft to cover the defect, and 23 (9%) had a combination of flap surgery and mesh graft. Autologuos nerve grafts (from the suralis nerve) were transplanted in 12 (4%) patients, and 24 (9%) patients received either artificial or autologous vascular grafts to bridge major defects. Table 3 details surgical complications after curative surgery.

Surgical Complications During and After Curative Surgery17

Table 3: Surgical Complications During and After Curative Surgery17

Postoperative radiation therapy was given to 164 (62%) patients. Seventy-one (27%) patients were treated with multiagent chemotherapy, whereas 1 (4%) underwent preoperative locoregional chemotherapy by isolated limb perfusion. Median follow-up was 40 months (range, 0–134 months). Seven patients were lost to follow-up. Twenty-four (9%) patients developed local recurrences that were proven by biopsy or magnetic resonance imaging. Thirty-eight (14%) patients developed metastases. Forty-eight (18%) patients had died of the disease at last data accrual, and 5 (2%) patients had died of other causes. No significant decrease existed in patients needing revision surgery after external surgical treatment over time (Figure 1).

Chart showing incidence of initial surgery according to guidelines per year.

Figure 1: Chart showing incidence of initial surgery according to guidelines per year.

Statistical Analysis

A stepwise multivariate Cox regression analysis was calculated, including covariables with a P value less than .1 in the univariate procedure. The AJCC and grading variables were considered as metric variables. A case-matched series was created for overall survival between groups A and B. Survival data were entered into a computerized database and analyzed. Patients were matched for tumor size, histological grading, depth, AJCC score, sex, and age. For categorical data, frequencies with percentages were used, and cross tabulations (2-tailed Fisher’s exact test and chi-square test) were used to assess the relationship between them. Age was reported as mean±SD; for all other continuous variables, the median was used with the range. Wilcoxon rank sum test was used to determine the statistical significance of group differences. Survival time was analyzed with Kaplan-Meier survival time analysis and a log rank test to assess differences in survival functions. All computations were done using the SPSS version 15 software (SPSS Inc, Chicago, Illinois). A P value less than .05 was considered significant.

Results

Prognostic Factors

Univariate and multivariate analysis revealed that AJCC score, grading, and age had the highest influence on survival (Figures 24). Adjuvant treatment with multiagent chemotherapy, which was mostly applied in high-grade sarcoma, also showed statistical significance (Tables 4, 5). Resection margins for curative surgery were wide in 93%, and resection status in accordance with histological grading was adequate in 97.7%. Statistical analysis did not show that surgical margins have an influence on survival, although occurrence of a metastatic lesion at some point after curative surgery was a significant negative prognostic parameter (P<.0001).

Kaplan-Meier estimator of grading, (G3–4, including subgroup of dedifferentiated sarcoma).

Figure 2: Kaplan-Meier estimator of grading, (G3–4, including subgroup of dedifferentiated sarcoma).

Kaplan-Meier estimator of occurrence of metastases at some point after curative resection.

Figure 3: Kaplan-Meier estimator of occurrence of metastases at some point after curative resection.

Kaplan-Meier estimator of American Joint Committee on Cancer score. Scores of 3 and 4 are taken together.

Figure 4: Kaplan-Meier estimator of American Joint Committee on Cancer score. Scores of 3 and 4 are taken together.

Univariate Cox Regression of Prognostic Parameters

Table 4: Univariate Cox Regression of Prognostic Parameters

Multivariate Cox Regression of Prognostic Parameters

Table 5: Multivariate Cox Regression of Prognostic Parameters

Prereferral Surgery

To compare patients with or without re-resection, 2 groups were created. Group A (n=135) was initially treated according to current guidelines. Group B (n=131) underwent surgery that did not comply with these guidelines, with subsequent reoperation at the authors’ institution. Most patients in group B underwent so-called “whoops” procedures.20

Comparison of Groups A and B

Demographic Data. The men:women ratio was 1.11:1 in group A and 1.26:1 in group B. Mean age at curative surgery was 58 years in group A and 55 years in group B. Mean time from the first medical appointment to curative surgery was 23 weeks in group A and 58 weeks in group B, with a high statistical significance (P<.001).

Primary Lesion. Mean primary lesion size was 11 cm (range, 1–34 cm) in group A and 8 cm (range, 1–30 cm) in group B (P<.001). Significantly more patients had tumors larger than 5 cm in group A (84%) than in group B (66%) (P=.002). The percentage of tumor localizations under the superficial fascia was higher in group A (85%) than in group B (55%), with a high statistical significance (P<.001). The pattern of histological grading was similar in both groups, with 54% of high-grade tumors in group A and 53% in group B (P=.758). Mean AJCC score was significantly higher in group B (P<.001). No difference existed regarding histological subtype, anatomical localization, or quality of initial symptom. Size of the primary lesions larger than 5 cm, location under the fascia, and AJCC score were potentially confounding variables between the groups of patients at baseline.

Surgery. Primary surgical therapy (biopsies excluded), regardless of where it was performed, was found on histology to be intralesional in 86% and marginal in 14% of patients in group B and intralesional in 0% and marginal in 4% (2 patients with low-grade liposarcoma) of patients in group A. Table 2 lists the sites of initial surgical therapy (biopsies excluded). Direct wound closure after resection or re-resection of the tumor or tumor bed was feasible in 60% of patients in group A and in 34% of patients in group B (P<.001). Twenty-one (88%) of 24 patients receiving mesh graft (12 together with flap surgery and 12 as a single reconstructive procedure) were in group B (P>.001), as were 31 (62%) of 50 patients undergoing flap surgery. The prevalence of surgical complications was similar in both groups (group A, 40%; group B, 62%; P=.852). Neither the severity of complications (according to Goslings and Gouma18) nor the number of surgical revisions were statistically different (Table 3).

Adjuvant Therapy. Thirty-two (26%) patients in group A and 40 (31%) patients in group B received multiagent chemotherapy, with no statistical difference (P=.221). One-third (43/135; 32%) of patients in group A received neoadjuvant multiagent chemotherapy before curative surgery, as did one-eighth (17/131; 13%) in group B (including 1 patient with isolated limb perfusion). Although radiotherapy was applied more often in group B (71%) than in group A (57%), no statistical difference existed (P=.167).

Survival. Mean and median survival were equal in groups A and B (mean, 64 vs 65 months, respectively; median, 61 vs 66 months, respectively). Forty-two (74%) patients in group A and 43 (73%) in group B were alive with no evidence of disease at their latest follow-up. Two patients in each group were alive with reported local recurrences, and 5 patients were alive with known metastases in group A, whereas all patients with reported metastases in group B died. Cumulative survival was higher in group A, but without statistical significance (P=.159) (Figure 5). Matched-case series for age, size, depth, and grading showed no significant differences in survival between the 2 groups.

Kaplan-Meier estimator of initial surgery according to guidelines with wide resection margins and initial surgery not according to guidelines without wide resection margins.

Figure 5: Kaplan-Meier estimator of initial surgery according to guidelines with wide resection margins and initial surgery not according to guidelines without wide resection margins.

Discussion

Approximately every second patient referred to the authors’ institution had already undergone surgery that did not conform to current guidelines. This patient cohort had smaller lesions that were mostly seated subcutaneously. They had to wait longer for definitive surgery and showed a higher rate of plastic reconstructive surgery at the site of resection. Survival, local recurrence rate, and incidence of distant metastases were equal to those in patients who underwent wide resection first.

Although current international criteria were applied to histological examination, a lack of detailed information on microscopic margins (eg, thickness in mm and quality of surrounding tissue) can be seen as one of this study’s shortcomings. Concise analysis of quality of life and functional scores would have contributed to better evaluation of the influence of prereferral surgery. Different anatomical localizations, different adjuvant therapy protocols, and unavailable information on prereferral status in patients with inadequate surgery precluded a statistical survey of these parameters. Compared with the estimated incidence of soft tissue sarcoma for the catchment area of the authors’ institution, less than 50% of all patients were treated at the institution. This may lead to bias because reluctance to follow guidelines is reported to increase with patient age, so such patients would have been referred to the institution less frequently.6 The study’s strength lies in the prospective data acquisition. The authors did not include a historical cohort with obsolete treatment modalities. Patients were treated according to current clinical guidelines at a single institution in a relatively short period.

The percentage of prereferral surgery in the literature ranges from 10% to 70%, but few studies focus on the influence of re-resection on parameters other than local recurrence, distant metastases, or survival.13 This may be due to similar survival rates after wide re-resection. The current study focused on the effect of prereferral surgery and of re-resection on the clinical course beyond recurrence or survival. Patients not initially treated at tertiary referral centers are left in the dark longer about their diagnosis and further treatment options.9,11 The need for wide resection of potentially contaminated tissue in reoperations leads to more extensive and mutilating surgery with a higher need for reconstructive plastic surgery,13 with functional impairment and high cost as logical consequences. Patients in the re-resection group had a significantly higher AJCC scores without impact on survival, with respect to the whole study population or when groups were matched for AJCC score. These findings are in accordance with the literature, where similar or longer survival has been reported in cases of re-resection.7

In analyzing prereferral clinical course, so-called “whoops” procedures predominated.21 These interventions are known to have a high incidence of marginal or intralesional resection margins with a high risk of recurrence and subsequent re-resection.12 Most of these patients were initially seen by a general practitioner and—apart from those not reported—surgically treated at so-called primary institutions. This is because most benign soft tissue lesions (eg, lipomas) are treated in these institutions. This is where awareness and referral practice should be improved. The key to reduction of the incidence of re-resections lies in better communication between primary institutions and increased awareness on the part of referring physicians.

Conclusion

Initial inadequate surgery for soft tissue sarcoma leads to an unfavourable clinical course but without a negative effect on survival after wide re-resection. More effort should be made to improve awareness and referral modalities for general practitioners and physicians at community hospitals.

References

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Site of Initial Surgical Interventiona

Site No. (%)
Study center 112 (42)
University clinic 19 (7)
District hospital 20 (8)
Community hospital 68 (26)
Doctor’s office 14 (5)
Not reported 33 (12)

Histology of Study Population

Histology No. (%)
Liposarcomaa 67 (25.2)
Undifferentiated pleomorphic sarcoma 54 (20.3)
Leiomyosarcoma 40 (15.0)
Myxofibrosarcoma 33 (12.4)
Synovial sarcoma 26 (9.8)
Malignant schwannoma 9 (3.4)
Primary extraosseous Ewing’s sarcoma 4 (1.5)
Epitheloid cell sarcoma 4 (1.5)
Parosteal osteosarcoma 4 (1.5)
Fibromyxosarcoma 4 (1.5)
Miscellaneous 21 (7.9)
Total 266 (100)

Surgical Complications During and After Curative Surgery17

Surgical Complication Score Definition No. (%)
0 No surgical complication 190 (71)
1 Temporary disadvantage, no [re-]operation 22 (8)
2 Recovery after [re-]operation 36 (14)
3 Permanent damage/disability 18 (7)
4 Surgery-related death 0 (0)
5 Unclear due to untimely death 0 (0)

Univariate Cox Regression of Prognostic Parameters

Parameter No. of Patients With Valid Data Hazard Ratio Standard Error of Estimate P
Age, y 240 1.027 0.00939 .0051
AJCC score 216 2.165 0.16146 <.0001
Multiagent chemotherapy 239 2.95 0.28682 0.0002
Grading 213 3.43 0.30722 <.0001
Grading 3 vs 1 213 19.9 1.01393 0.0032
Metastases 240 7.301 0.29678 <.0001
Lung metastases 240 6.197 0.29983 <.0001
Neoadjuvant multiagent chemotherapy 238 2.186 0.35607 .028

Multivariate Cox Regression of Prognostic Parameters

Parameter No. of Patients With Valid Data Hazard Ratio Standard Error of Estimate P
Grading 184 2.703 0.37521 .008
Metastases 184 3.656 0.34115 .0001
Multiagent chemotherapy 184 3.448 0.41493 .0029
Age, y 184 1.051 0.01526 .0012

10.3928/01477447-20120725-22

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