Pelvic Reconstruction with a Structural Pelvic Allograft After Resection of a Malignant Bone Tumor

Delloye, Christian MD, PhD; Banse, Xavier MD, PhD; Brichard, Bénédicte MD, PhD; Docquier, Pierre-Louis MD; Cornu, Olivier MD

Journal of Bone & Joint Surgery - American Volume: March 2007 - Volume 89 - Issue 3 - p 579–587
doi: 10.2106/JBJS.E.00943
Scientific Articles

Background: Reconstruction of the pelvic arch after resection of a malignant pelvic tumor remains a major surgical challenge because of the high rate of associated complications. The purpose of this investigation was to assess the functional outcome and complication rate following treatment with a bone allograft to reconstruct the pelvis.

Methods: Twenty-four consecutive patients underwent excision of a malignant pelvic bone tumor and reconstruction with a pelvic bone allograft. The living patients were followed for a minimum of twenty-four months. There were nineteen primary malignant bone tumors, sixteen of which were high-grade sarcomas, and there were five isolated metastases. Patients were examined clinically and radiographically and were assessed functionally with the Musculoskeletal Tumor Society score.

Results: The mean age of the patients at the time of the index surgery was thirty-four years, and the mean duration of follow-up was forty-one months. Eighteen of the twenty-four resections involved the periacetabular area and were followed by reconstruction either with a hip prosthesis (thirteen) or with an osteochondral allograft alone (five). The six other resections involved the iliac bone. All patients received a massive bone allograft that had been sterilely procured without secondary irradiation. At the time of our last evaluation, eight patients were alive and free of disease. Seven patients had a local recurrence. Neurological deficits were present in six patients, and three had a deep infection. Nonunion of three of the sixteen allografts that could be evaluated was observed. Neither graft fracture nor lysis was observed. Eleven patients underwent surgical revision, with nine of these revisions related to the reconstruction. The average Musculoskeletal Tumor Society score at the time of the latest follow-up was 73% of the maximal possible score. The average score was 82% for the eleven patients with an age of less than twenty years at the time of the index procedure and 65% for the thirteen older patients. Ten patients walked without any assistive device, and five of them had normal function with no or only a slight limp.

Conclusions: Pelvic reconstruction after a limb-sparing resection is associated with a high risk of surgical complications and usually should be reserved for patients with a primary bone sarcoma. A pelvic allograft can restore the anatomy and provide good functional results, especially in young patients. Nonunion was the most common allograft-related complication.

Level of Evidence: Therapeutic Level IV. See Instructions to Authors for a complete description of levels of evidence.

1 Divisions of Orthopaedic Surgery (C.D., X.B., P.-L.D., and O.C.) and Pediatric Oncology (B.B.), Department of Surgery, Cliniques Universitaires St.-Luc, 10, avenue Hippocrate, B1200 Brussels, Belgium. E-mail address for C. Delloye: delloye@orto.ucl.ac.be

Article Outline

Tumors in the pelvic area remain a major challenge. In the past, most malignant tumors in the pelvis were treated with hindquarter amputation1. With improvements in chemotherapy, limb-preserving procedures have gradually emerged as a viable surgical modality2 and, in most cases, have now replaced ablative surgery. Because the anatomy of the pelvis is complex, extensile exposure is a surgical challenge and there is a need to identify and preserve major neurovascular structures. Pelvic surgery is characterized by a high number of complications3-8. Enneking and Dunham3,5, Erikson and Hjelmstedt4, and Steel6 were among the first surgeons to report their results with limb-sparing surgery after excision of a bone tumor of the pelvis. These procedures were most disabling when the acetabulum was excised. Despite the high morbidity and mortality, these authors demonstrated that, with an adequate margin, a number of patients can survive. Hindquarter amputation or limb-sparing resection without periacetabular reconstruction is nowadays less acceptable as the expected function is poorer than that obtained with reconstructive surgery9,10.

Johnson11 advocated reconstruction of a pelvic defect with a prosthesis and cement. Today, a prothesis12-17 and bone both can be used as implants in a pelvic reconstruction. The resected bone can be autoclaved17,18 or irradiated19 before it is reimplanted. The transfer of a bone autograft from the proximal part of the femur is another option20. However, bone allograft2,21-24 is the currently preferred material for reconstructing a pelvis with or without the use of a prosthesis.

One of the major advantages of bone allografts is that the bone can be shaped and customized in order to match the pelvic resection. The complex osseous architecture can be fully restored for locomotion, avoiding a flail hip or an arthrodesis. However, there are few available data on the outcome of pelvic allograft procedures. Their use remains quite controversial because they are associated with high rates of infection and mechanical failure16,18,22.

We report our experience with twenty-four consecutive patients who underwent reconstruction with a pelvic bone allograft following a pelvic resection. This study was performed in order to assess the functional outcome and the surgical complications of this mode of reconstruction.

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Materials and Methods

Clinical Series

From 1985 to 2003, twenty-four consecutive patients underwent resection of a malignant tumor of the pelvis followed by reconstruction with a massive bone allograft that had been harvested from the pelvis of an organ donor. Patients were informed about the planned surgery and the existing alternatives and gave their consent. Institutional approval was obtained for this study.

There were nine women and fifteen men with a mean age (and standard deviation) of 34 ± 23 years (range, eight to seventy-six years) at the time of the index surgery. Table I lists the diagnoses and the surgical staging of the tumors. There were nineteen primary bone tumors and five metastatic lesions that were considered to be isolated at the time of the index surgery. Ewing sarcoma was the predominant lesion. Figure 1 shows the distribution of the pelvic tumors in the surgical areas (zones I through IV) defined by Enneking and Dunham5. Of the twenty-four tumors, eighteen (thirteen primary tumors and five metastases) involved the acetabular region (zone II). The six other tumors were located at the ilium (zone I alone or with zone IV). The topographical distribution is indicated in Table II.

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Oncological and Surgical Procedures

Neoadjuvant and adjuvant chemotherapy was given to seventeen patients. One patient had received preoperative radiation therapy. En bloc removal of the tumor with wide margins was the aim of the surgery. Most patients had a preoperative cleansing intestinal preparation. All patients had the operation under general anesthesia. Ureteral stents were placed in selected patients. Cephalosporin was administered prophylactically until no bacterial growth on culture of intraoperative specimens of the allograft was reported. The operations were performed with the patients in a three-quarter position (semisupine and semi-lateral), maintained by bags and rolls allowing anterior and posterior positions.

All except two procedures were performed through an extended ilioinguinal approach, from which there was a lateral extension to the proximal part of the femur, achieving an iliofemoral exposure. This approach allowed extensive visualization of the inner and outer aspects of the hemipelvis5. In two patients with a tumor in zones I and IV, no femoral extension was necessary, but the approach was extended at the spine by a T-shaped incision.

The surgical margins that were achieved were classified, on the basis of the surgical and pathological reports, according to the system described by Enneking et al.25 as radical, wide, marginal, or intralesional.

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Reconstructive Procedure

All osseous resections were followed by anatomic reconstruction with a bone (obtained from the local nationally registered bone bank) that was similar to the one that had been resected. Pelvic allografts were sterilely procured in an operating room from organ donors by a surgical team26. The average age of the donors at the time of death was 40 ± 13 years (range, fourteen to sixty-two years; median, forty-two years). Bones were immersed in serum with rifampicin (1.2 g/L of serum) for one hour before being frozen at –80°C until use. The mean preservation time was 13 ± 12 months (range, 0.5 to thirty-eight months). No final irradiation for sterilization was performed. At the time of the surgery, the allograft was thawed for about one hour in a rifampicin solution at 37°C.

Allografts were fixed by one or preferably two molded 3.5-mm ASIF reconstruction plates (Synthes, Brussels, Belgium) in the periacetabular area and/or with one or two 6.5-mm lag screws in the sacrum and/or one screw in the pubic ramus. In thirteen patients, a cemented total hip prosthesis that included a cemented polyethylene cup and a 22.2 or 28-mm metallic head was implanted to restore the hip joint (Figs. 2-A and 2-B). In five patients, the acetabular component of the allograft matched the femoral head of the patient and the hip joint was restored without a prosthesis (Figs. 3-A and 3-B). All spared muscles were attached when possible to the pelvic allograft. Three patients were treated with traction for three weeks, as the hip was considered to be unstable at the time of surgery, and two others were treated with an anti-dislocation device for eight weeks after an episode of prosthesis dislocation. The remaining patients were not treated with immobilization postoperatively. Weight-bearing was not allowed for two months, to allow soft-tissue healing. After two months, patients were allowed to walk with two crutches and progressive loading on the operatively treated limb. Adjuvant chemotherapy, if any, was resumed at three weeks postoperatively.

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Functional Evaluation

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Patient function was assessed according to the Musculoskeletal Tumor Society (MSTS) criteria27. Pain, functional capacity, walking distance, use of a support, gait, and emotional acceptance were each evaluated on a 5-point scale, with a maximum total score of 30 points recorded as 100%. Patients who had received two successive allografts were assigned two separate scores for function. The follow-up period was calculated from the time of surgery to the last consultation, to the time of allograft removal, or until the patient's death. Living patients were analyzed at a minimum of twenty-four months postoperatively.

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Statistical Analysis

Nonparametric testing was performed with the SPSS statistical package (version 12.0; SPSS, Chicago, Illinois). The Mann-Whitney U test was used to compare two unpaired subgroups of patients according a grouping variable such as the location of the resection, an age of less than twenty years or an age of twenty years or older, whether palsy had occurred, surgical revision, and union or nonunion. These subsets were compared with regard to the duration of surgery, the blood loss, the MSTS score, and the hospital stay. Relationships between two sets of parameters were analyzed with use of the Spearman rank order correlation coefficient. The level of significance was set at p < 0.05.

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Results

The duration of follow-up ranged from one to 137 months, with an average of forty-one months. Every living patient in the series was followed for a minimum of twenty-four months. The main data on the patients are listed in a table in the Appendix.

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Surgical Procedures

The mean duration of the complete surgical procedure (from the induction of the anesthesia until the patient was taken from the operating room) was 10 ± 2.8 hours (range, 4.5 to 16.5 hours). The average compensated blood loss during the hospital stay was 4359 ± 2800 mL (range, 1000 to 11,300 mL). The amount of blood loss correlated with the duration of the surgery (r = 0.44; p = 0.03) but not with the duration of the hospital stay, patient age, or the area of bone resection (zone II compared with not zone II). The mean hospital stay was 25 ± 18 days (range, ten to ninety-four days) and correlated strongly with patient age, with older patients having the longest stay (r = 0.61; p = 0.001), but not with the duration of the operation. Tissue culture of allograft specimens obtained at the time of the surgery were negative, except for two cases of late growth of Peptostreptococcus or Corynebacterium. Intravenous antibiotic therapy was discontinued after one week except for the two patients with positive cultures, who were treated for three weeks. A clinical infection did not develop in either of those two patients. Adjuvant chemotherapy was resumed at three weeks for fourteen patients and was delayed for three others because of skin necrosis or infection.

The surgical resection included the periacetabular area (zone II) in eighteen patients. Those patients did not differ significantly from the patients without acetabular resection with regard to age, operative time, hospital stay, or amount of blood transfused, with the numbers available (Table II). Five patients, with a mean age of 15 ± 5 years, had an osteoarticular allograft that allowed sparing of the femoral head. In thirteen other patients with a periacetabular excision (mean age, 46 ± 22 years), the hip was restored with a cemented hip prosthesis. The sacroiliac joint was resected in four patients and was replaced with an allograft and an arthrodesis, usually with fixation with two screws. In two patients, the three zones (I, II, and III) were resected and reconstructed. All except three of the resections disrupted the pelvic arch. The surgical resection was wide in nineteen patients, marginal in six, and intralesional in one.

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Oncological Aspects

Eight (33%) of the twenty-four patients were alive and free of disease when they were last seen, at a mean of seventy months. Thirteen patients (54%) had died of the disease, and there were three deaths not related to the malignant tumor. A local recurrence was observed in seven patients (29%), two of whom underwent hindquarter amputation.

Of the nineteen patients with a primary bone tumor, six were alive without evidence of disease at a mean of 62 ± 40 months postoperatively. In this group with primary sarcoma, a local recurrence occurred in seven patients after a mean time of 21 ± 19 months. Of the five patients with a solitary bone metastasis located in or next to zone II, two survived without evidence of disease for an average of ninety-five months. There were two deaths unrelated to the tumor and no local tumor recurrence.

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Surgical Complications and Morbidity

There was one early postoperative death from a pulmonary embolism at four weeks. The morbidity rate was high (Table III). One patient had a femoral artery thrombosis diagnosed in the immediate postoperative period; this required vascular revision, which was complicated by a compartment syndrome necessitating additional surgery. Two patients had skin necrosis, and there were three deep infections. We found no relationship between infection and either blood loss or the duration of the surgery, with the numbers available.

Neurological complications and hip dislocation or subluxation were observed only in the eighteen patients with a zone-II resection (Table III). Sciatic nerve palsy occurred in six patients, who had only partial recovery. One of these patients also had a femoral nerve palsy. Patients with neurological deficits had a significantly longer duration of the operation (p = 0.022) than did those without a deficit. Hip complications were observed in five patients. Two hip prostheses dislocated. Two femoral heads gradually subluxated from an acetabulum reconstructed with an osteochondral allograft and were left untreated. One femoral fracture occurred distal to the prosthetic stem, and it was treated with a plate.

Of the twenty-four patients, eleven (46%) had a total of sixteen surgical procedures to treat a complication of the surgery and nine underwent a surgical revision related directly to the reconstruction itself. Thirteen patients (54%), with a mean age of twenty-five years at the time of the index operation, had no surgical revision; these patients were younger than the eleven patients who required revision (average age, forty-four years; p = 0.031).

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Evaluation of Bone Allografts

Sixteen allografts could be evaluated radiographically for healing, as they were in patients who had been followed for at least eighteen months. An unhealed junction after that period was considered to be a nonunion21.

There were forty-three anastomotic junctions with host bone, and five of them (12%) failed to unite by eighteen months postoperatively. Two nonunions were revised with new allografts, which also failed to unite. Nonunion was not found to be significantly associated with the age of the patient, duration of the surgery, or amount of blood transfused, with the numbers available. Hardware failure was observed in two patients with a nonunion and in a third patient in the immediate postoperative period.

No resorption or lysis and no fracture of the graft were observed in this series. Seven allografts had an uneventful course for at least three years, and four of them had an uneventful course for five years. Of the five patients who had had a hip joint reconstruction with an osteoarticular allograft, two subsequently had progressive dislocation of the femoral head with wear of the acetabular roof.

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Functional Evaluation

The Musculoskeletal Tumor Society (MSTS) score could be determined for twenty-three patients who had a total of twenty-five allografts, as one patient had died one month postoperatively. The mean MSTS score was 21.5 ± 6 points (73% of the maximal possible score)27. The MSTS score was found to be inversely correlated with patient age (r = –0.58; p = 0.002) as well as with the duration of the operation (r = –55; p = 0.007). The eleven patients who were less than twenty years of age had an average score of 24.7 ± 7 points (82% of the maximal score) whereas the older patients had an average score of 19 ± 5 points (65% of the maximal score). This difference was significant (p = 0.016).

All except four patients were able to walk. The patients who could walk had an average MSTS score of 23 points (78% of the maximal score). Three patients needed two crutches for walking, five patients occasionally used one crutch, and two routinely used one crutch. Ten patients walked without any device, and five of them had normal function with no or only a slight limp and an unlimited walking capacity. The walking performance of the eleven patients who were younger than twenty years old was excellent; eight of the children walked without support, two of them occasionally used a crutch, and one was unable to walk.

The six patients with a reconstruction in zone I or in zones I and IV had an average MSTS score of 26 ± 3.8 points, whereas the seventeen with a reconstruction in zone II alone or in combination with one or more of the other zones had an average score of 20.4 ± 6.6 points. With the numbers available, this difference was not significant (Table II).

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Discussion

When excision of a pelvic tumor and reconstruction have been combined in one procedure, the reported complication rate has been high, ranging from 30% to 90% in series ranging in size from nine to ninety-six patients8,13-17,19,22-24,28,29. Carter et al.1 reported that a hindquarter amputation without reconstruction was associated with a 41% complication rate in a series of thirty-four patients. The reported durations of operations that included both pelvic resection and pelvic reconstruction have been high, ranging from five to ten hours8,10,14,22,24, with blood loss ranging from 2500 to 8300 mL depending on the extent of the reconstruction8,10,14,17,22. The data in our study are consistent with those findings.

There were no perioperative deaths in our series, and the postoperative mortality rate was low. The femoral artery thrombosis that occurred in a patient with Ewing sarcoma resulted from prolonged excessive traction during a lengthy procedure and might invoke the question of whether surgery is the best option to control a radiosensitive tumor. Studies dealing with pelvic Ewing sarcoma have had conflicting results; the impact of surgery on overall survival could not be verified in some of them30-32, whereas others have indicated that surgery combined with chemotherapy tends to offer better local control and survival than any other combination of treatments without surgery33-40. Surgery should be considered only when the tumor can be completely removed. The role of surgery for less radiosensitive tumors, such as osteosarcomas, and for nonresponsive tumors, such as chondrosarcomas, is more obvious4,5,41,42.

Neurological problems were the most frequent surgical complications, with a prevalence of 25%, and were exclusively observed in patients with a periacetabular resection (zone II). The reported rate has ranged from 3% to 30% in series ranging in size from nine to ninety-two patients7,10,13,16,28,29. Most palsies were complete and partially resolved; full recovery was not the rule in our series. According to Capanna et al.7,41, neurological complications are predominant following iliac resections with disruption of the greater sciatic notch.

Limb-sparing surgery has become accepted standard surgical treatment for primary bone sarcoma unless the lesion cannot be surgically removed in an appropriate manner. Wide resection and reconstruction remain a questionable approach for a solitary bone metastasis in zone II of the pelvis, where curettage, cementation, and the placement of a supportive ring and prosthesis have been reported to have good results43. In patients with metastatic carcinoma, the risks can outweigh the expected benefit of a wide resection. A potentially curative reconstruction appears not to be the procedure of choice in this circumstance, except for an isolated metastasis that is resistant to radiation therapy and chemotherapy43. Limb-sparing surgery exposes the patient to a tumor resection with narrower margins than are achieved with a hindquarter amputation, which also does not guarantee eradication of the local disease1,23. In studies of limb-salvage procedures in series ranging in size from thirty-five to ninety-two patients, the local recurrence rate has ranged from 28% to 35%13,15,28,41,42; the rate in our study is within that range.

There is no unanimous opinion regarding the most appropriate method of reconstruction. Periacetabular resection without reconstruction will result in pelvic instability44. Many authors8,10,45,46 have demonstrated that patients with a stable, reconstructed pelvis have better MSTS functional scores than do patients without pelvic reconstruction. Palliative surgery such as iliofemoral or ischiofemoral arthrodesis, although better than amputation, is less well accepted nowadays.

In zone II, there are several alternatives to an allograft reconstruction. The range of reconstruction techniques has been broadened by the development of new prostheses, new biomaterials9,12-14,29,47, and new surgical methods20. There are three current techniques for periacetabular reconstruction: insertion of a saddle prothesis14, use of a computer-aided-designed prosthesis to bridge the resection12,13,47, and a hip arthroplasty with cement and with or without11 the support of an autograft17,18,20 or an allograft18,23,24. The advantage of a saddle prosthesis is modularity and ease of reconstruction14. The other techniques are more complex as the reconstruction must fit the resection. The use of bone, whether autograft or allograft, allows the surgeon to implant a conventional total or bipolar prosthesis and to match a potentially greater resection than anticipated. A total hip arthroplasty with cement was preferred in our series because wear of the allograft was a potential concern with the use of a bipolar prosthesis48.

Infection is a major surgical complication of pelvic reconstruction, regardless of the method of reconstruction. Its prevalence has ranged from 0% to 37% in series ranging in size from nine to ninety-six patients8,13-17,19,22-24,28,29,46. Ozaki et al.22 and Hillmann et al.46 reported a 37% infection rate in their respective series of twenty-two and thirteen patients treated with a pelvic allograft, which would indicate that this procedure is an unacceptable choice. Such a high rate was not found by others23,24 nor by us in the present study. This discrepancy remains unclear but may be related to the procurement of the allograft. We could not confirm the finding by Hong Tan and Mankin49 that blood loss influenced the infection rate. Impregnation of the allografts with rifampicin at the time of procurement and at implantation has decreased the rate of contamination of bone allografts in our experience26. Bone has been shown to be an appropriate carrier of antibiotics that will be released from the time of implantation and for at least twenty-one days50-52.

Fracture and nonunion are concerns with the use of allograft or irradiated bone and autograft16,19,22-24. In our study, nonunion occurred in three young adult patients with a high activity demand. In two of them, the allograft was inadequately matched with the host bone, leaving a large interfragmentary gap. Cutting and adjusting a hemipelvic graft to fit the area of osseous resection was one of the most difficult steps in the reconstruction and was most challenging in zone II. Selection of a size-matched pelvic allograft remains a concern. Another difficulty is related to fixation in the ilium, which can be tenuous. We observed two nonunions in this location. Gaps and narrow surfaces at the junctions were both concerns associated with nonunion. We believe that there is a need for a computer-assisted osteotomy in tumor resection and in cutting of the bone allograft in order to achieve a better match of the allograft to the resection.

Another concern associated with bone allografts is the potential transmission of viral diseases53,54. Procedures have been designed to ensure the supply of safe tissues. These include guidelines for donor selection, tissue quarantine, and tissue processing. The risk of transmitting a communicable disease remains remote with the implementation of quality systems in tissue banks and specific procedures for safety such as back-screening and nucleic acid testing of organ and tissue donors.

We advocate the use of a pelvic allograft instead of bones from another skeletal location. This allows true anatomical restoration of the complex architecture of the pelvis and leaves open various options for hip preservation, particularly in children.

Anatomical reconstruction following a pelvic resection provides the opportunity for much better function than does palliative reconstruction. The range of function as calculated as the percentage of the maximum MSTS score (normal function) ranged from 55% to 70% in series ranging from thirteen to thirty-nine patients9,13,23,24. In series of patients in whom the pelvis was reconstructed with either an allograft or a prosthesis16,46, the allografts compared favorably with the prostheses in adults as well children. We reported an average MSTS score of 73%, confirming the possibility of obtaining an anatomically and biomechanically sound reconstruction with an allograft. More than half of our twenty-four patients walked without crutches or only occasionally used one crutch. In our series, as in a previous one16, children and teenagers performed substantially better than adults, with an average score of 82% compared with 65%. Ten of the eleven children walked without support or with only occasional use of a crutch. Whether this was due to their age or to a lesser extent of revision surgery could not be determined.

The rate of complications of limb-sparing pelvic resection is high. Today, limb-sparing surgery with reconstruction is preferred to amputation when possible13,23,28,41, but it should usually be reserved for primary sarcoma. We believe that, when such reconstruction is anticipated, a pelvic allograft should be considered, especially in young patients, in whom very acceptable function can be expected.

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Appendix

A table showing clinical details regarding all twenty-four patients is available with the electronic versions of this article, on our web site at jbjs.org (go to the article citation and click on “Supplementary Material”) and on our quarterly CD-ROM (call our subscription department, at 781-449-9780, to order the CD-ROM). ▪

Disclosure: The authors did not receive any outside funding or grants in support of their research for or preparation of this work. Neither they nor a member of their immediate families received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, division, center, clinical practice, or other charitable or nonprofit organization with which the authors, or a member of their immediate families, are affiliated or associated.

Investigation performed at the Cliniques Universitaires St.-Luc, Brussels, Belgium

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