Limb salvage, where indicated, is now the norm for a large majority of bone tumors. The advent of effective neoadjuvant chemotherapy has made limb salvage an oncologically safe option without compromising long-term survival. Although there is considerable literature on surgical excision for local control in appendicular lesions, series documenting the results of surgery in pelvic tumors especially in the pediatric population are not so common 1–5. Pelvic tumors, besides being uncommon, offer a unique challenge to adequate oncologic resection because of their location, large size at presentation, and close proximity to neurovascular structures and visceral organs 6–8. Reconstruction after resection to minimize functional morbidity is also demanding and the immature skeleton has its own specific problems. The poor prognosis in pelvic tumors as compared with extremity lesions, prolonged surgical time with associated blood loss, and the possibility of postoperative complications associated with pelvic resections are some of the other potential complications that make surgical treatment of these lesions challenging 6,8–10.
The purpose of this study was to evaluate the morbidity, functional outcome, and oncologic results in pediatric patients with malignant tumors of the pelvis treated with surgical resection as part of their multimodality treatment.
Patients and methods
We reviewed 639 malignant skeletal tumors in patients 18 years and younger who were treated with limb salvage at our institute over a 9-year period between November 2000 and December 2009. These included 30 patients with malignant tumors of the pelvis who had undergone surgical resection. The patients were identified by a retrospective review from a prospectively maintained database. The medical records, imaging, oncologic, and functional status were reviewed. There were 20 males and 10 females, mean age 13 years (range 2–18 years) (Table 1). Twenty-seven patients presented to our institute primarily and three were referred after an attempted incomplete excision elsewhere.
Tissue diagnosis was obtained or reviewed in all the cases. The diagnosis included Ewing sarcoma in 22 patients, osteogenic sarcoma in four, chondrosarcoma in two, and synovial sarcoma of bone in two. Before surgery, all patients were subjected to a thorough oncological assessment to determine the extent of local disease and exclude the presence of distant metastases. Staging studies, including plain radiographs and MRI of the limb, CT scans of the chest, total body scintigraphy, and bone marrow biopsies, where indicated, were carried out. In the latter part of the series, PET scan was used as part of the staging investigations in patients with Ewing sarcoma. All patients were nonmetastatic at presentation. Indicated patients received chemotherapy and radiotherapy according to the existing hospital protocol.
MRI was used to define the extent of the lesion, the involvement of the soft tissues, relation to the neurovascular bundle, and the level of transection of the bone. The primary goal of surgery was complete excision of the tumor, with preservation of a functional limb. The decision to offer surgical excision to these patients was taken at a multidisciplinary tumor board meeting on the basis of the possibility of achieving tumor-free resection margins as evaluated on preoperative imaging. Pelvic resections were classified according to Enneking and Dunham into four types: iliac (T1), acetabular (T2), pubis or ischium (T3), and sacral (T4) (Fig. 1) 11. Combinations of these resections were also carried out. After resection, various methods of reconstruction were adopted. These were based on the type of resection, individual surgeon preference, and the functional specifications of the patient as assessed during preoperative counseling.
Eighteen resections included resection of the acetabulum (T1+T2=11, T2+T3=5, T1+T2+T3=1, T1+T2+T4=1) and 12 did not include resection of the acetabulum (T1=8, T1+T4=3, T3=1). No reconstruction was carried out in the 12 patients in whom resection excluded the acetabulum (Fig. 2). An arthrodesis was carried out in three patients, extracorporeal radiation and reimplantation in four, and a pseudarthrosis in 11. For pseudarthrosis, we performed a hip transposition, stabilizing the femoral head to either the sacrum, residual ilium, or ischium using a prolene mesh to create a pseudocapsule (Fig. 3) 12,13.
The resected specimens were evaluated for surgical margins and to assess the histological response to chemotherapy wherever applicable. On the basis of the evaluation of tumor necrosis after preoperative chemotherapy, the histologic response was considered good when the extent of tumor necrosis was 90% and above and poor when the necrosis was less than 90%.
Patients were asked to attend follow-up every 3 months for the first 2 years and 6 monthly subsequently. Twenty-seven patients were available for follow-up. Follow-up was determined from the time of diagnosis to the last date of review or death. Besides screening for disease surveillance, radiographs of the local part were assessed at each visit. Functional status was assessed at the time of the last follow-up using the Musculoskeletal Tumor Society Scoring system 14.
Overall survival rates were analyzed using the Kaplan–Meier method. Survival time was taken from the date of diagnosis to the last date when the patient was documented to be alive or the date of death.
The duration of surgery ranged from 165 to 525 min (mean 300 min). Surgeries requiring acetabular resection and reconstruction lasted longer (mean 348 min) compared with surgeries in which the acetabulum was retained (mean 218 min). The average blood loss was 1390 ml (range 200 to 5500 ml).
Two of 30 patients had involved margins. Of the 26 patients in whom histologic response to chemotherapy was assessed, 19 patients showed a good response to chemotherapy and seven were poor responders. Five patients with Ewing sarcoma had postoperative radiotherapy (four poor responders and one good responder with a very large soft tissue component).
Two patients died because of chemotherapy complications at 6 and 4 months, respectively (Cases 22 and 27).
One patient had an intraoperative urethral injury, two had wound dehiscence that required secondary suturing, and three had infection. Of these three patients with infection, wound lavage was adequate for resolution in two. The other patient had a persistent discharging sinus till he succumbed to disease at 16 months (Case 12). One patient had an intraoperative sacrifice of the L5 S1 nerve roots as they were enmeshed in disease (Case 25). Three other patients had common peroneal nerve palsy that did not recover. One patient in whom the femoral head was stabilized to the residual acetabulum after a partial resection involving the acetabulum had increasing hip stiffness progressing to painless ankylosis (Case 15).
Three patients were lost to follow-up at 49, 46, and 8 months, leaving 27 patients available for follow-up. All the patients lost to follow-up were disease free at the time of the last review. The follow-up in all patients ranged from 4 months to 138 months (mean 43 months).
There were two local recurrences. One of these occurred in a case with involved margins (Case 8). She also had distant disease recurrence and died at 5 months. The other was in a patient with chondrosarcoma in whom incomplete excision had been attempted before being treated at our institute. This patient also had distant disease recurrence and died at 18 months (Case 4).
Histologic response to chemotherapy was assessed in 26 patients. Sixteen of 19 patients with a good response to chemotherapy were available for follow-up. One of these patients died because of chemotherapy complications, one succumbed to disease, and 14 are currently alive with no evidence of disease. Of the seven patients with a poor response to chemotherapy three succumbed to disease and four are currently alive with no evidence of disease.
Thus, 19 patients are currently alive (14 good responders, four poor responders, and one in whom chemoresponse was not assessed), 17 being free of disease.
The follow-up of the survivors ranged from 24 to 138 months (mean 55 months). Overall survival for all patients was 68% at 5 years (Fig. 4).
The functional status was determined at the last follow-up using the Musculoskeletal Tumor Society scoring system. This was based on the analysis of three factors (pain, functional activities, and emotional acceptance) pertinent to the patient as a whole and three factors specific to the lower limb (use of supports for ambulation, walking ability, and gait). For each of the six factors, values of 0–5 were assigned on the basis of established criteria. The result was expressed as a sum total with a maximum score of 30 and as a percentage of the expected normal function for the patient. The Musculoskeletal Tumor Society Score (MSTSS) was available for all survivors. The score ranged from 22 to 29. As expected, patients in whom the acetabulum was retained had better function (mean score 27) as compared with patients in whom the acetabulum was resected (mean score 25).
Pelvic tumors are much rarer than extremity lesions 15. Less than 5% (30 of 639) of limb salvage surgeries in the pediatric population at our institute were for pelvic tumors. Resection and reconstruction of pelvic tumors is far more challenging than extremity lesions 3. Besides the danger of injury to neurovascular structures and visceral organs because of their close proximity, surgical complications include infection, leg length discrepancy, hematoma, delayed healing, and skin problems, which can affect up to 50% of patients in some series 16. The superiority of limb salvage surgery over an amputation in maintaining the patient’s image of body integrity and enhancing limb function is well documented 15. Hence, if oncologically safe resection is possible, then a higher complication rate in complex limb salvage and reconstructive procedures may be acceptable 15. The type of reconstruction modality used varies according to the anatomical location, extent of resection, and individual surgeon preference.
Our low rate of local recurrence (7%) indicates that we were able to achieve adequate local margins in our patients, thus justifying the oncologic safety of pelvic resections in appropriate patients. This could be an indication of the fact that unlike earlier series that spanned many decades, this is a recent series. Advances in imaging technology help the surgeon plan surgical margins with greater accuracy than in earlier eras 15. Another possible factor as suggested by Gebert et al. 12 may be the lack of prosthesis or allografts as a reconstruction modality in our patients. Free from the constraints of being dependent on a custom-made endoprosthesis or on a chosen allograft, the resection can be carried out without being overly concerned about the reconstruction. If there has been significant tumor growth since the last imaging, the surgeon has the flexibility to widen the resection margin on the basis of intraoperative findings.
We had three cases of infection that required a lavage. The 10% infection rate is lower than that reported in other series 4,15,16. This could partly be attributable to the fact that 40% of the patients in our series did not undergo any form of reconstruction. There were no pelvic allografts and in only seven of 18 reconstructions were metallic implants used 17,18. Hip transposition using available soft tissues and a prolene mesh for stabilization of the femoral head minimizes the presence of foreign material in the wound. The absence of grafts and prosthesis for reconstruction reduces the tissue bulk and facilitates a tension-free skin closure, thus decreasing the incidence of wound complications.
Some authors advocate reconstructing T1 resections to re-establish pelvic integrity 3,15,19. We did not reconstruct any of the resections that excluded the acetabulum. Our MSTSS of 90% in these cases indicates that these patients function well even in the absence of reconstruction. Similar observations have been made by others too 20. Our MSTSS of 83% in patients with acetabular resections is higher than that in other series 16. The fact that patients in our series were children or young adults could have been the reason for this 12. It is well established that children adapt to functional limitations better 16. Limb length discrepancy affecting gait was not uncommon 5,12,15. We did not carry out any limb-lengthening procedures. Most patients adapted adequately with a shoe raise and even enthusiastically participated in sporting activity. Patients uniformly reported good psychological acceptance despite having a compromised gait as a result of inadequate abductor muscle function, which is inevitable, either because of loss of abductor musculature and/or loss of the fulcrum (resection of the acetabulum).
Our overall survival of 68% at 5 years is comparable with other series of surgically operated pelvic tumors 5,15. Our oncologic results in pelvic tumors are not inferior to those obtained in our series of extremity tumors, thus belying the belief that pelvic tumors have a poorer prognosis 21,22. Other authors have also reported similar findings on comparing pelvic and extremity tumors 12,23.
Our series has its limitations. It is a retrospective review. The etiology of the lesions is varied. A longer follow-up may result in late related surgeries for complications from pelvic limb salvage 24. Some authors have reported deterioration in functional outcomes especially in emotional acceptance, whereas others have suggested that the scores do not deteriorate with time 12,25.
Despite these shortcomings, we believe that this study does add to the increasing understanding of the outcome of surgically treated pelvic tumors in the pediatric population. As the literature on the results of malignant pediatric pelvic tumors is sparse, we believed that it was justified to present the results of our heterogeneous group in an attempt to aid better understanding of these lesions. Its strength also lies in the fact that it presents the results of a group of patients who were managed by the same multidisciplinary team. The cases were seen and treated at a specialist oncology center over a relatively short period of time, where treatment philosophy was consistent and not affected by the availability of various investigational and therapeutic modalities in different eras.
The oncologic outcomes of pediatric patients with malignant tumors of the pelvis treated with surgical resection as part of their multimodality treatment are very encouraging. Although these are challenging surgeries, with their inherent complications, the ultimate functional outcomes are good.
Conflicts of interest
There are no conflicts of interest.
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