Osteoarticular allograft versus prosthetic allograft composites: which reconstruction method results in superior outcomes following the resection of proximal femur tumor in adolescent and preadolescent patients?

Abstract

Background

Primary malignant tumors of the proximal femur in children are rare, and there is no consensus about the optimal reconstruction method for this condition. While methods for biological reconstruction—such as vascularized fibular allograft and rotationplasty—and nonbiological options like expandable endoprosthesis exist as reconstructive choices, each method has its distinct advantages and disadvantages. In this study, we compared the outcomes of osteoarticular allograft (OAA) with allograft-prosthetic component (APC) in reconstructing the proximal femur in a cohort of adolescent and preadolescent patients.

Patients and methods

Twenty patients aged between 8 and 13 years with primary malignant bone tumors of the proximal femur who were managed with either OAA or APC reconstruction were included. The median follow-up was 71 months (range 24–140). The primary outcome of interest was limb function evaluated by the Musculoskeletal Tumor Society (MSTS) score. Secondary outcomes of interest were surgical complications.

Results

The median MSTS score of the patients was 23 (range 20–25) in the OAA group and 26 (range 23–27) in the APC group (P = 0.003). Postoperative complications in the OAA group included two nonunions (18.1%), two infections (18.1%), six degenerative joint diseases (54.5%), and one allograft fracture (9.1%). The postoperative complications in the APC group included one nonunion (11.1%), one dislocation (11.1%), and two allograft fractures (22.2%). Allograft fractures were managed with revision and replacement with a tumor prosthesis. No revision was done to address the DJD in the OAA group.

Conclusion

OA and APC reconstructions of the proximal femur following tumor resection in adolescent and preadolescent patients each have their benefits and associated complications. However, APC reconstruction appears to provide superior limb function and a lower incidence of postoperative complications.

Introduction

Malignant bone tumors account for 6% of all malignancies in skeletally immature populations [1]. Osteosarcomas and Ewing’s sarcomas are the most common types of these tumors, comprising 56% and 34% of pediatric malignant bone tumors, respectively [1]. The femur is the most common site for malignant bone tumors, with a frequency of almost 42% [2]. In the femur, nearly 75% of the malignant bone tumors occur in the distal portion, and involvement of the proximal femur is relatively rare, particularly in the pediatric population [2]. For this reason, the outcomes of proximal femur malignant tumors in pediatrics have been scarcely reported, and the optimal reconstruction method for these tumors is largely unknown.

Reconstruction of the proximal femur using an expandable prosthesis is often linked to a high incidence of postoperative complications and failure [3, 4]. Bio-expandable prostheses, although introduced as a solution for limb length discrepancies in children, have notable drawbacks, including bone loss at the implant fixation site and the need for multiple revision surgeries [5]. Consequently, biological reconstruction of the proximal femur presents a valuable alternative for adolescent and pre-adolescent patients.

Ratationplasty remains a viable biological reconstructive option, offering reasonable local control and functional outcomes [6]. However, it is limited by unconventional limb appearance [6]. Osteoarticular allograft (OAA) and allograft-prosthetic composite (APC) are among the available biological methods for reconstructing the femur in pediatrics, despite their inherent risks, such as fracture, nonunion, and infection [7, 8]. Compared to expandable prostheses, they preserve bone stock, facilitating future revisions when necessary. In addition, they provide structural support, with tendons and capsules acting as anchors for abductor muscle attachment and residual host capsule integration [9]. This limitation has been addressed to some extent in expandable prostheses by using Trevira tubing to enhance soft tissue attachment and stability [10].

Although allograft reconstruction can lead to limb length discrepancies in skeletally immature patients, this issue can be partially addressed by choosing an allograft that exceeds the size of the bone defect, thereby allowing for some length compensation as bone growth continues [11]. However, this approach has its own risks, such as nerve palsy and skin problems caused by tension. Therefore, the optimal method of reconstruction following the resection of proximal femur tumor in adolescent and preadolescent patients remains unclear.

In this study, we present the clinical, functional, and oncologic outcomes, along with postoperative complications associated with the use of OAA and APC for reconstructing the proximal femur in a cohort of adolescent and preadolescent patients.

Methods

This retrospective cohort study was approved by our institute’s review board. Medical profiles of skeletally immature patients who underwent a proximal femur reconstruction in our tertiary hospital between January 2000 and May 2022 were reviewed. Inclusion criteria were pathologic diagnosis of a malignant primary bone tumor of the proximal femur, age between 8 and 13 years, reconstruction with an OAA or APC, and a minimum follow-up of two years. Patients who had hip joint involvement or distant metastases at presentation, patients who were treated for tumor recurrence, patients who were lost to follow-up, and those who died within two years of operation were excluded from the study. Hip joint involvement was considered if effusion was observed in MRI. The reason for setting an age limit for this study was that in our center, patients younger than 8 years are generally managed with a vascularized fibular allograft, while patients older than 13 years are managed with an endoprosthesis.

The final analysis included 20 patients who met the study criteria. Reconstruction was done with OAA in 11 patients and APC in 9. The flow diagram of the patient’s inclusion and exclusion is demonstrated in Fig. 1. Sonography-guided core needle biopsies were performed for all patients. In two patients with Ewing’s sarcomas, the results were inconclusive, and an incisional biopsy was performed for a definitive diagnosis. All patients received pre-operative and postoperative chemotherapy based on the standard protocols.

Fig. 1

Flow diagram of the study

Patients

The study population included 11 (55%) males and 9 (45%) females with a median age of 11 years [8, 9, 10, 11, 12, 13]. The primary bone tumor type was osteosarcoma in 55% (n = 11) and Ewing sarcoma in 45% (n = 9). The median resection length was 17 cm [14, 15, 16, 17, 18, 19, 20]. The median follow-up was 71 months (24–140). No significant difference was observed between the characteristic features of the patients in the OAA and APC reconstruction group (Table 1).

Table 1 Comparison of the characteristic features between the two study groups

Surgical procedure

All the surgeries were done by one senior orthopedic oncologist. Our primary reconstruction option was OAA. To this purpose, we initially tried to find an allograft that matched the patient’s acetabular size on preoperative radiographs. In some cases, we successfully identified an allograft that closely approximated the patient’s acetabulum. However, in certain instances, an allograft that appeared suitable on preoperative imaging did not provide an adequate fit intraoperatively, necessitating a shift to APC. Additionally, when a radiographically matched allograft was unavailable at the time of surgery, APC reconstruction was planned as an alternative approach.

After general anesthesia, patients were positioned laterally. The incision extended from 4 cm proximal to the greater trochanter, encompassing the elliptical biopsy tract and extending distally for an appropriate length. We cut the tensor fascia lata and detached the abductor’s tendon from the greater tuberosity and the proximal quadriceps muscle from the lesion with adequate margin. Based on a T1-weighted MRI, osteotomy of the femur was performed with a margin of at least 2 cm. A frozen section of the remaining distal bone marrow was evaluated to ensure it was tumor-free. We raised the proximal femur and detached the muscles and joint capsule. A matched-sized OAA was obtained from our university bone bank, which harvests allografts using standard tissue banking protocols. The allografts were stored at -85 °C for at least two weeks before implantation [12]. The graft size was typically chosen to be at least 2 cm longer than the defect. After that, we attempted to insert the head of the allograft into the acetabulum. The medullary canal of the allograft was reamed and filled with bone cement to reinforce structural integrity and reduce the risk of future fractures. A dynamic compression plate was used to fix the allograft in place with at least two screws that passed through the neck to augment it. The plate bridged the entire length of the allograft (Fig. 2). In cases where the femoral head does not appropriately fit into the acetabulum (Fig. 3), the neck of the OAA was cut as per the standard hip arthroplasty procedure. A bipolar femoral component (Zimmer Biomet, Warsaw, Indiana, USA) with the appropriate head size was then cemented into the medulla of the allograft. Finally, the component was fixed to the remaining femoral shaft with a dynamic compression bridging plate (Figs. 4 and 5). The capsule and abductor muscle remnants in the OAA group and abductor muscle remnants in the APC group were sutured to the allograft with a nonabsorbable thread.

Fig. 2

(A, B) Anteroposterior and lateral radiograph of an 11-year-old girl with Ewing sarcoma of the proximal left femur after neoadjuvant chemotherapy; (C) coronal T2 weighted MRI showing the medullary extension of the tumor; (D, E) Anteroposterior and lateral radiograph three years after wide resection and reconstruction with osteoarticular allograft showing osteoarthritis

Fig. 3

Intraoperative photograph showing a femoral head not fitting into the acetabulum

Fig. 4

Intraoperative photograph displaying reconstruction using an allograft prosthesis composite

Fig. 5

(A, B) Anteroposterior and lateral radiograph of a 13-year-old girl with osteosarcoma of the proximal right femur after neoadjuvant chemotherapy; (C) coronal T2 weighted MRI showing the medullary extension of the tumor; (D) Anteroposterior radiograph two years after wide resection and reconstruction with allograft prosthesis composite

Postoperative protocol follow-up

For all patients, a hip abduction brace was used for six weeks after the operation. Toe-touch weight-bearing was initiated two days after the operation; Partial weight-bearing was encouraged three weeks after the operation, and full weight-bearing was allowed after the union of the allograft to the host bone. The follow-up visits were every three months for the first two years, every six months for the first five years, and yearly afterward for up to ten years. At each follow-up visit, the patients were evaluated clinically for pain, limping, range of motion, dressing needs, use of walking aids, walking capacity, sitting capacity, stair climbing ability, and return to sports activities. Radiological assessments were conducted at each follow-up visit, including radiographs of the affected area and chest CT scans, to monitor surgical and oncological outcomes and identify any complications.

Outcome evaluation

Outcome measures were recovered from the patient’s medical records. Clinical outcomes were a range of motion (ROM) and limb function at the last follow-up. Clinical outcomes are not reported for the patients who had local recurrence within two years of the operation (n = 2). Hip ROM, including flexion and abduction, was assessed using a standard goniometer. Limb function was evaluated by the Musculoskeletal Tumor Society (MSTS) score for the lower extremity, containing six subscales of pain, function, emotional support, walking, and gait, each scoring on a 0–5 scale, comprising a total score of 0–30. MSTS scores were extracted via a chart review, with higher scores indicating a better function [13].

Radiologic outcomes were bony union at the host-allograft junction and the development of degenerative joint disease (DJD). The union of the allograft-host junction was defined as the observation of callus formation and periosteal sclerosis between the allograft and the host bone, and there was no radiolucent line [14]. DJD was categorized into four grades (I-IV) using the Kellgren-Lawrance classification system [13].

Oncologic outcomes included the assessment of local and distant recurrence, which were extracted for the medical records. Two fellowship-trained orthopedic surgeons who were not involved in patient care evaluated all outcome measures. In case of disagreement between the two observers, the senior author adjudicated the disputes.

Statistical analysis

IBM SPSS for Windows, version 28 (IBM Corp., Armonk, N.Y., USA) was used for statistical analyses. Descriptive data are presented with a median and range for quantitative variables or a number and percentage for qualitative variables. A Mann-Whitney U test was used to compare quantitative variables between the two study groups. Qualitative variables were compared using a chi-squared or Fisher’s exact tests. A p-value < 0.05 was considered significant.

Results

Clinical outcomes

The median hip flexion was 97.5º (90–120) in the OAA group and 95º (90–110) in the APC group (P = 0.33). The median hip abduction was 30º (20–40) in the OAA and 27.5º (20–35) in the APC group (P = 0.29). The median MSTS score of the patients was 23 (20–25) in the OAA group and 26 (23–27) in the APC group (P = 0.003).

Patient-reported outcomes

At the last follow-up, none of the patients in either group required a walking aid. In the OAA group, five patients reported mild pain, all attributed to DJD. In the APC group, one patient experienced mild pain. The pain was managed with NSAIDs in all patients.

Four patients in the OAA group and one in the APC group exhibited slight limping, which did not require intervention. Additionally, three patients in the OAA group and one in the APC group had some difficulty with stair climbing. Despite these issues, all patients were able to perform daily activities, such as putting on socks, shoes, and pants. Six patients in the OAA group and eight in the APC group returned to limited sports activities, including cycling and swimming. The patient’s reported outcomes are demonstrated in more detailes in Table 2.

Table 2 Comparison of patient outcomes measures between the osteoarticular allograft (OAA) versus allograft-prosthetic composite (APC)

Radiologic outcomes

Union of the host-allograft junction was observed in 9 of 11 (81.8%) patients in the OAA group and 8 of 9 (88.8%) patients in the APC group (P = 0.466). The median time to union was nine months [6, 7, 8, 9, 10, 11, 12] in both groups (P = 0.94).

Oncologic outcomes

Local recurrence was recorded in two (18.2%) patients in the OAA group and one (11.1%) in the APC group. The time to recurrence was 18 and 30 months after the operation in the OAA and 18 months after the operation in the APC group. Local recurrences were managed with amputation and chemotherapy. Lung metastasis was observed in two (18.2%) patients in the OAA group and two (22.2%) in the APC group. Metastasis was managed with mastectomy and chemotherapy. At the final follow-up, 9 of 11 (81.8%) patients in the OAA and 7 of 9 (77.7%) patients in the APC group were still alive. Two patients in the OAA group and one patient in the APC group died within two years of the operation due to widespread metastasis and were excluded from the study according to the study criteria.

Postoperative complications

Nonunion of the host-allograft junction was observed in two (18.2%) patients in the OAA group and one patient (11.1%) in the APC group; it was managed by an autogenous bone graft from the ipsilateral ilium. At the final follow-up, DJD was detected in 6 of 11 (54.5%) patients in the OAA group, which were grade II (Fig. 2) in four patients and grade III in two patients. No intervention was done for these patients. Protrusi acetabulum did not occur in any patient of the APC group. Infection was recorded in two (18.2%) patients in the OAA group and not in the APC group. One of them was superficial and managed by intravenous antibiotics. The other one was a deep infection, which occurred two weeks after the operation. It was managed by irrigation and debridement allograft-retaining procedure.One dislocation happened in the APC group eight weeks after the operation. Dislocation was managed by closed reduction and six weeks of spica cast immobilization. None of the patients in either group experienced allograft lysis (Table 3). A noticeable limb length discrepancy (> 1 cm) was observed in two patients from each group. However, the discrepancy was minimal and did not require any intervention.

Table 3 Postoperative radiologic, oncologic, and surgical complications of proximal femur reconstruction using osteoarticular allograft (OAA) versus allograft-prosthetic composite (APC)

Failure

Two allograft fractures occurred in the APC group 28 and 32 months after the operation versus one allograft fracture in the OAA group 34 months after the surgery. All fractured allografts were replaced by tumor prostheses. Postoperative radiologic, oncologic, and surgical complications of the patients in the two study groups are summarized in Table 3.

Discussion

Reconstruction of the proximal femur in young people following tumor resection requires distinct considerations compared to adults, as it must preserve bone stock for future revisions while accommodating ongoing skeletal growth [15]. Both biological methods—such as vascularized fibular grafts [16] and rotationplasty [6]—and non-biological options, including expandable prostheses [3, 4], can be considered for this purpose. However, the optimal reconstruction method in this population is less discussed, mainly due to the rare incidence of these tumors in skeletally immature children. In this study, we compared the functional outcomes, surgical complications, and failure rate of the two methods for reconstructing the pediatric proximal femur, including OAA and APC reconstruction.The limb function was significantly inferior in patients managed with OAA. Moreover, the postoperative complications were considerably more in the OAA group. The main postoperative complication in the OAA group was DJD. Although DJD causes mild pain in the majority of patients, with longer follow-up, we would expect most of the OAA joints to become more arthritic and lead to joint replacement or endoprosthesis.

Case series and cohort studies on proximal femur reconstruction in skeletally immature patients are quite limited. In 2003, Belthur et al. reported the use of extensible endoprostheses for the reconstruction of the proximal femur following the tumor resection in nine children with a mean operative age of 10.2 years. The mean MSTS score was 77.6% in four patients who were alive in the last follow-up [17]. In the present study, the median MSTS score was 23 (76.7%) for OAA and 216 (86.7%) for the APC group. This data shows that biological reconstruction could provide similar or even superior functional outcomes compared to expandable prostheses.

Seven out of nine (77.7%) patients in the study by Belthur et al. had a revision or a major complication, mainly due to acetabular loosening and hip dislocations [17]. In the present study, only three (15%) mechanical failures were recorded, all for allograft fractures. These observations imply that biological reconstruction of the proximal femur in adolescent and preadolescent patients could be associated with less surgical failure compared to expandable prostheses.

Although biological reconstruction of the proximal femur in adolescent and preadolescent patients generally experiences fewer mechanical failures, it is still susceptible to its own set of complications. Nonunion is a frequent complication of allograft reconstruction [11]. In this study, we had three nonunions (15%), two in the OAA group and one in the APC group. DJD is also a frequent complication of OAA, so all pediatric patients who are managed with OAA could expect the development of DJD at some point [11]. In this study, six (54.5%) patients in the OAA group developed various degrees of DJD within a median follow-up of 72 months. However, no protrusi acetabulum was recorded in patients managed with APC. Although no revision was made for DJD in the present study, the patients will require conversion to total hip arthroplasty later. Therefore, it can be concluded that APC reconstruction of the proximal femur is a more reasonable procedure in skeletally immature patients who outlive their disease. A smaller complication rate of APC versus OAA reconstruction was also reported earlier (29% vs. 42%) [18]. OAA reconstruction just gives patients time to grow old enough for endoprosthetic replacement.

Limb length discrepancy could be regarded as a source of dissatisfaction following the resection of the proximal femur in young patients [19]. To address this issue and improve patient satisfaction, we selected an allograft that was 2 cm longer than the defect, minimizing the risk of limb length discrepancy as much as possible. As a result, a noticeable limb length discrepancy (> 1 cm) was observed in only four patients in this study (two in each group), highlighting the relative success of this approach.

The length of resection and the amount of soft tissue removed both impact postoperative function [20]. In this study, resection lengths were comparable between the OAA and APC groups, and since the extent of soft tissue removal generally correlates with resection length, these factors remained consistent across both groups. Although resection lengths were comparable between the two groups, functional outcomes differed significantly, favoring APC reconstruction. This discrepancy may be attributed to several factors. First, the native joint surface in OAA reconstruction is replaced with an allograft, which lacks living cartilage and has limited capacity for biological integration, predisposing patients to DJD and reduced mobility. In contrast, APC reconstruction incorporates a prosthetic component that provides better joint congruency and stability, contributing to superior function. Additionally, differences in soft tissue reattachment may have influenced outcomes. APC reconstruction may allow for more stable reattachment of the abductor muscles and joint capsule, enhancing hip function and reducing limping. Furthermore, the higher incidence of DJD in the OAA group likely contributed to pain and stiffness, further impairing functional recovery. These factors collectively explain the superior functional outcomes observed in the APC group despite similar resection lengths. While DJD typically causes mild pain initially, prolonged follow-up suggests that many OAA joints may become increasingly symptomatic, potentially necessitating joint replacement or endoprosthetic conversion [11].

This study was not without limitations. The main limitation of this study was its retrospective design, which makes it prone to several types of bias, including selection bias, transfer bias, and mis-assessment bias. Finally, the small number of patients in both groups might have significantly impaired the statistical analysis results. Therefore, the results of this study should be interpreted in the context of these limitations..

Conclusion

OAA and APC reconstructions are both viable procedures for adolescent and pre-adolescent patients undergoing proximal femur resection for primary bone tumors. Both techniques provide acceptable functional outcomes. Compared to APC, OAA is associated with a higher risk of postoperative complications, particularly DJD.