Abstract
Objective
To evaluate the result of en bloc resection and reconstruction of the distal radius with a non‐vascularized fibular autograft for giant cell tumor (GCT) of bone.
Methods
Between 2005 and 2015, 12 eligible patients (seven males, five females, mean age 31.3 years) with grade III GCT of the distal radius were treated by en bloc resection and reconstruction with non‐vascularized proximal fibular autografts in four Chinese institutions (members of Giant Cell Tumor Team of China). The patients had a clinical and radiographic review every 6 months for the first 2 years then annually thereafter. The functional, oncologic and radiological outcomes of the patients were analyzed.
Results
The mean duration of follow‐up was 39.6 months. Bony union was achieved in all cases. None of the patients were dissatisfied with the shape and appearance of the wrist. The mean MSTS score was 25.23 ± 2.38 (range, 22–29). The mean DASH score was 13.0 (range, 6.7–33.3). The average range of motion of the wrist was: 35.8° ± 14.5° of extension, 14.0° ± 8.4° of flexion, 15.5° ± 6.7° of radial deviation, 19.4° ± 10.1° of ulnar deviation, 57.2° ±18.9° of pronation and 44.0° ± 24.8° of supination. The average percentage of grip strength was 55.2% ± 29.0% compared with that of the contralateral side. One localized soft tissue recurrence occurred; it was successfully managed by excision. Lung metastases developed postoperatively in one case and were treated by gamma knife radiotherapy. There was radiographic evidence of radiocarpal arthritis in eleven patients, bone resorption in ten, distal radioulnar joint diastasis in six, ulnar deviation of the wrist in seven, subluxation of the carpal bone in three and dislocation of the carpal bone in one patient.
Conclusions
Reconstruction with a non‐vascularized proximal fibular autograft is a reasonable option after en bloc resection of the distal radius for giant cell tumor of bone.
Keywords: Distal radius, En‐bloc resection, Giant cell tumor, Non‐vascularized fibular autograft
Introduction
Giant cell tumor (GCT) of bone is a benign locally aggressive tumor and tends to recur. After the distal femur and proximal tibia, the distal radius is the third most common location of this tumor1, 2, 3, 4. Of note, a high rate of recurrence in this location has been widely recognized, the high rate being attributable to several factors, including anatomic geometry of the distal radius, complexity of the distal radioulnar joint, the paucity of surrounding muscle, and the close proximity of critical nerves, arteries and tendons5, 6, 7, 8. Therefore, GCT of distal radius comprises a distinct subgroup of tumor that is difficult to manage.
The goal of treatment for GCT involving the distal radius has always been to achieve a negligible local recurrence rate while preserving as much normal anatomic structure and joint function as possible. However, this goal may be difficult to attain in patients with advanced stage disease, which always presents with ill‐defined borders, cortical destruction and soft‐tissue extension. Many surgeons prefer to managing advanced lesions by en bloc resection and reconstruction of the distal radius9, 10, 11. Although the techniques for resection have been similar, those for reconstruction have varied. Reconstruction with a non‐vascularized proximal fibular autograft has many advantages over other techniques. It achieves satisfactory functional and cosmetic results and is relatively free of major complications9, 12, 13. Reconstruction with a non‐vascularized proximal fibular autograft is therefore widely performed. To date, there have been a number of single institution studies on the outcomes of reconstruction with fibular autografts14, 15, 16. However, to the best of our knowledge, there are no multicenter studies on this subject from China.
Therefore, the Giant Cell Tumor Team of China (GTOC) performed this retrospective study to (i) evaluate the clinical and radiographic results of en bloc resection and reconstruction of the distal radius with non‐vascularized fibular autografts for GCT; and (ii) to assess the reasons for the incongruity between subjective and objective results.
Materials and Methods
The seven Chinese institutions that participated in this study are members of the GTOC and frequently collaborate on research on topics of mutual interest. All these centers have musculoskeletal tumor clinics and have similar approaches to GCT management and patient rehabilitation.
This study was carried out with the approval of each institution's review board.
We searched the hospital records of every center for patients who had undergone treatment for GCT of the distal radius between June 2005 and July 2015. Patients treated by en bloc resection and reconstruction with non‐vascularized autogenous fibular grafts were included in this study. Those with local recurrence of GCT at initial presentation, than 6 months of follow‐up, or no perioperative radiographs available were excluded.
Forty‐four patients treated by wide excision and reconstruction with non‐vascularized autogenous fibular grafts were initially included in this study; subsequently 22 patients were excluded on the basis of the above exclusion criteria. Of the 22 eligible patients, 12 agreed to return for personal interviews and evaluation. Five of the remaining 10 patients who did not return for follow‐up could not be reached and the other five refused to participate in this study.
The 12 patients being analyzed comprised seven males and five females with a mean age of 31.3 years at the time of surgery (SD, 11.6 years; range, 16–59 years).
All patients were routinely evaluated preoperatively with plain radiographs (Fig. 1), CT and MRI scans of the involved forearm and CT of the chest, after which they were all classified according to the Campanacci staging system for GCT of bone1. Additionally, serum calcium, phosphorus and alkaline phosphatase concentrations were routinely measured to rule out hyperparathyroidism. Core needle biopsies were then performed if the lesion was atypical clinically or radiologically.
Figure 1.

Preoperative plain radiographs (anteroposterior and lateral views) showing a typical osteolytic and expansile lesion of the left distal radius that is characteristic of GCT.
The surgical approach was chosen on the basis of the location of the tumor and the preference of the treating surgeon. The biopsy tract, if present, was removed in the initial incision. En bloc resection of the distal radius was then performed with a safe margin (Fig. 2), after which the proximal fibula was excised as previously reported13, 14. The fibular graft was then placed into the forearm and fixed to the proximal radius with a compression plate or one‐third tubular plate. K‐wires were utilized to stabilize the newly reconstructed joints, if necessary (Figs 3, 4). Next, the remnant fibular collateral ligament was sutured to the radial collateral ligaments to increase the stability of the joints.
Figure 2.

Photographs of operative specimens after en bloc resection of the distal radius had been routinely performed with a safe margin. Of note, the distal radius was sectioned 3 cm proximal to the proximal extent of the tumor.
Figure 3.

Intraoperative fluoroscopy images (anteroposterior and lateral views) showing fixation with K‐wires, multiple cortical screws and plate; desirable alignment of the newly built wrist joint has been achieved.
Figure 4.

(A) Postoperative X‐ray film (anteroposterior view) showing the contralateral knee joint from which the proximal fibular graft has been obtained. (B) Immediate postoperative X‐ray film demonstrating good alignment of the newly reconstructed wrist joint.
After surgery, a long arm splint was applied for 8–10 weeks. At 10–12 weeks, the K‐wires were removed (Fig. 5) and a short arm splint applied until radiological union had been achieved. Strong use of the wrist and hand was forbidden for a whole year.
Figure 5.

Postoperative X‐ray film (anteroposterior view) demonstrating the K‐wires have been removed 10 weeks after surgery; there is no apparent bone union.
The patients had a clinical and radiographic review every 6 months for the first 2 years and annually thereafter. Imaging (X‐ray, CT, with/without MRI) of the surgical site and chest were routinely performed. Additionally, complications at the donor site such as peroneal nerve palsy and ligamentous insufficiency were also recorded. The most recent follow‐up data were used for analysis.
Function was evaluated by Disabilities of the Arm, Shoulder, and Hand scores (DASH)11, 17 and the revised functional evaluation system of the Musculoskeletal Tumor Society (MSTS)18. In addition, grip strength was measured with a dynamometer and range of motion (ROM) of the wrist measured with a goniometer and compared with the contralateral side.
All radiographic images of the forearm and chest were reviewed by experienced surgeons and imaging physicians to determine whether bony union, recurrence, metastasis of tumor or complications had occurred. Of note, radiocarpal arthritis was assessed according to the grading system of Haus and Jupiter19. In this system, Grade 0 is defined as normal joint space, Grade 1 as slight joint space narrowing, Grade 2 as marked narrowing with osteophyte formation, and Grade 3 as bone‐on‐bone narrowing with osteophyte and cyst formation.
Results
General Results
Relevant patient characteristics and results are summarized in Tables 1 and 2.
Table 1.
Patient characteristics and outcomes
| Case | Sex | Age (years) | Grade | Pathological fracture | Origin of fibula | Fibular length (cm) | Follow‐up (months) | Recur | Range of motion (°) | Grip strength (%)* | MSTS score | DASH score | |||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| RD | UD | FL | EX | Pro | Sup | ||||||||||||
| 1 | F | 29 | III | — | Ipsilateral | 7.5 | 44 | — | 30 | 17 | 25 | 40 | 50 | 17 | 30 | 25 | 20.8 |
| 2 | M | 25 | III | — | Contralateral | 6 | 9 | — | 18 | 15 | 20 | 40 | 37 | 43 | 80 | 24 | 12.5 |
| 3 | M | 37 | III | — | Contralateral | 6 | 7 | — | 10 | 14 | 22 | 18 | 64 | 74 | 20 | 22 | 12.5 |
| 4 | F | 19 | III | Yes | Contralateral | 6 | 72 | — | 5 | 20 | 5 | 50 | 58 | 90 | 80 | 24 | 11.6 |
| 5 | M | 25 | III | Yes | Ipsilateral | 6.2 | 48 | — | 10 | 44 | 15 | 56 | 47 | 55 | 89 | 29 | 6.7 |
| 6 | M | 22 | III | Yes | Ipsilateral | 8 | 58 | — | 14 | 28 | 25 | 55 | 71 | 57 | 59 | 26 | 6.7 |
| 7 | M | 16 | III | — | Ipsilateral | 7 | 27 | Local | 17 | 15 | 20 | 21 | 77 | 10 | 0 | 23 | 33.3 |
| 8 | M | 35 | III | — | Ipsilateral | 5 | 19 | — | 25 | 30 | 6 | 45 | 63 | 58 | 25 | 29 | 8.3 |
| 9 | F | 31 | III | — | Contralateral | 8 | 12 | — | 15 | 10 | 10 | 15 | 20 | 45 | 60 | 22 | 17.5 |
| 10 | M | 38 | III | — | Ipsilateral | 6 | 31 | — | 15 | 10 | 10 | 25 | 80 | 10 | 80 | 26 | 8.3 |
| 11 | F | 59 | III | Yes | Ipsilateral | 5 | 28 | — | 15 | 10 | 0 | 25 | 80 | 40 | 60 | 27 | 6.7 |
| 12 | F | 40 | III | — | Ipsilateral | 6 | 120 | — | 12 | 20 | 10 | 40 | 40 | 30 | 80 | 26 | 11.6 |
EX, extension; F, female; FL, flexion; M, male; Pro, pronation; Recur, recurrence; RD, radial deviation; Sup, supination; UD, ulnar deviation.
Grip strength (%): percentage of the normal side.
Table 2.
Postoperative radiographic results
| Case | Degenerative arthritis (grade) | Bone resorption | Distal RUJ diastasis | Wrist ulnar deviation | Wrist dislocation |
|---|---|---|---|---|---|
| 1 | 2 | Yes | — | — | — |
| 2 | 1 | — | Yes | Yes | — |
| 3 | 0 | Yes | — | — | Palm Sx |
| 4 | 1 | Yes | Yes | Yes | — |
| 5 | 3 | Yes | — | Yes | — |
| 6 | 2 | Yes | Yes | — | — |
| 7 | 3 | Yes | Yes | — | Dorsal Dx |
| 8 | 3 | Yes | Yes | Yes | — |
| 9 | 1 | — | — | — | Palm Sx |
| 10 | 2 | Yes | — | Yes | — |
| 11 | 3 | Yes | — | Yes | — |
| 12 | 2 | Yes | Yes | Yes | Dorsal Sx |
Dx, dislocation; RUJ, radioulnar joint; Sx, subluxation.
Eight patients had left and four right distal radius involvement. All were classified as grade III tumors, according to the Campanacci staging system. Three patients had pathological fractures. None of the cases had metastatic disease at the time of diagnosis. The mean duration of follow‐up was 39.6 months (SD, 32.3 months; range, 7–120 months).
Core needle biopsies with either CT or C‐arm fluoroscopy guidance were performed preoperatively in five cases. In the other seven cases, preoperative imaging findings were characteristic of GCT and the diagnoses were confirmed postoperatively.
A dorsal approach was used in 11 cases and a volar approach in the remaining one. The ipsilateral fibula was used in eight patients and the contralateral fibula in the other fours. The mean length of fibula excised was 6.4 ± 1.0 cm (range, 5–8 cm). Radiological union was achieved in all cases (Fig. 6). No patient had peroneal nerve palsy or ligamentous insufficiency related to the donor site and none were dissatisfied with the shape and appearance of the wrist.
Figure 6.

CT scan images obtained 1 year postoperatively showing bony union, Grade 2 radiocarpal arthritis, and mild bone absorption.
Functional Results
At the most recent follow‐up, the mean MSTS score was 25.25 ± 2.38 (range, 22–29) and the mean DASH score 13.0 (SD, 7.5; range, 6.7–33.3). The average ROMs of the wrist were as follows (Fig. 7): 35.8° ± 14.5° (range, 15°–56°) of extension, 14.0° ± 8.4° (range, 0°–25°) of flexion, 15.5° ± 6.7° (range, 5°–30°) of radial deviation, 19.4° ± 10.1° (range, 10°–44°) of ulnar deviation, 57.2° ± 18.9° (range, 20°–80°) of pronation, and 44.0° ± 24.8° (range, 10°–90°) of supination. The average percentage of grip strength compared with that of the contralateral side was 55.2% ± 29.0% (range, 0–89.0%).
Figure 7.

Clinical photographs taken 1 year postoperatively showing satisfactory extension, flexion, supination and pronation of the wrist.
Oncologic Outcomes
A localized soft tissue recurrence was diagnosed 28 months after the initial operation in one patient (Case 7, Fig. 8). This patient was successfully managed by excision of the tumor (3 cm × 3 cm × 3 cm). Part of the impaired extensor pollicis longus tendon was also resected and reconstructed by transfer of an extensor tendon. The patient was followed up for another 6 months and remained disease‐free at the time of the last follow‐up. However, the ROM of his wrist and grip strength were poor (Table 1).
Figure 8.

Local recurrence in a 37‐year‐old man with GCT. (A) X‐ray film taken 28 months after the initial operation demonstrating dorsal dislocation of the carpal bones and (B) An abnormal soft tissue mass is evident near the proximal fibula; recurrence was confirmed.
Another patient developed lung metastases approximately 32 months postoperatively (Case 4) and was treated by gamma knife radiotherapy. She was symptom‐free with stable lung nodules when reviewed after 27 months.
Radiographic Evaluation
At the final follow‐up, 11 patients had radiographic evidence of radiocarpal arthritis. One of these was rated as Grade 0, three as Grade 1, four as Grade 2 and four as Grade 3 according to the grading system of Haus and Jupiter19. Various degrees of bone resorption were also observed in 10 patients. Distal radioulnar joint diastasis was present in six cases. Seven had ulnar deviation of the wrist, two had palm subluxation of the carpal bone with one dorsal subluxation and one dorsal dislocation (Figs 6, 8, 9).
Figure 9.

X‐ray films 12 years after the initial surgery demonstrating Grade 3 radiocarpal arthritis, distal radioulnar joint diastasis, ulnar deviation of the wrist and dorsal subluxation of the carpal bone.
Discussion
As is well known, GCT of bone is an aggressive tumor with a relatively high rate of recurrence. GCTs in the distal radius are reportedly more aggressive and metastasize more often to the lungs10, 20, 21. Additionally, most patients are young active adults who demand cosmetically acceptable and functionally adequate wrists9, 22. Treatment of GCT involving the distal radius therefore poses great challenges for the treating surgeons, who must weigh the extent of the surgical procedure and the subsequent functional deficit against the risk of recurrence to attain the goal of achieving a negligible local recurrence rate while maximizing musculoskeletal function2, 8.
Curettage and bone grafting or cementing to preserve the involved joint has traditionally been preferred for small lesions13, 23, 24. For high grade tumors, especially grade III tumors, the treatment is controversial. Some authors still advocate consideration of intralesional curettage and cementing whereas others have recently reported successfully treatment with only the monoclonal antibody denosumab5, 7, 25. Although controversial, en bloc resection is strongly recommended by most authors, especially in subjects with recurrence or pathological fracture or whose tumors have enlarged rapidly or are clearly malignant10, 26, 27. En bloc resection of the distal radius must be followed by meticulous reconstruction of the bone defect to preserve the wrist function and alignment.
Many techniques have been used to reconstruct the defects, including vascularized27/non‐vascularized fibular grafts28, 29, osteoarticular allografts30, partial/total wrist arthrodesis and custom‐made prostheses8, 10, 11, 14, 16, 28, 29, 30, 31, 32. Each technique has its own unique possible advantages and disadvantages, which has been thoroughly discussed and debated 11, 20, 27, 28, 30, 32, 33, 34. However, no consensus on the optimal procedure has yet been reached. Thus, treating surgeons select the reconstruction method on the basis of their own experience and preference.
Of note, reconstruction with non‐vascularized proximal fibular grafts has been widely utilized in many medical centers. However, most published studies have been conducted in single institutions with small number of patients. To date, no multicenter studies have been published on this subject in China. We therefore designed this multicenter study with the aim of evaluating this reconstruction procedure more comprehensively and objectively.
In this series, the functional, oncologic and radiological outcomes of 12 patients from four Chinese institutions were analyzed.
Functional Outcomes
This reconstruction option yielded acceptable functional results (Table 1) that are similar to those reported by other authors. Reported ROMs of the wrist have ranged from 28° to 32° of extension, 21° to 38° of flexion, 15° to 21° of radial deviation, 8° to 12° of ulnar deviation, 50° to 61° of pronation and 27 to 60° of supination. Mean reported MSTS scores are 25.9–27.92, 28, 29, 35. Although postoperative motion is inferior to normal wrist function, most patients were satisfied with their postoperative function. This apparent discrepancy may be partly explained by the concept of “functional range of wrist motion”. Palmer et al. used a triaxial electrogoniometer to measure functional wrist motion36 and concluded that most of our daily tasks require a minimum of wrist motion and that the “functional range of wrist motion” is between 5° of flexion, 30° of extension, 10° of radial deviation, and 15° of ulnar deviation. Brumfield et al. have also reported that the optimum functional motion of the wrist required to accomplish most activities is from 10° of flexion to 35° of extension37. In our series, the postoperative ROMs are well within the reported range. Secondly, as described by MacDermid and Tottenham, the upper limb functions as a unit for many activities of daily life38. Function of the impaired wrist may be partly compensated for by the adjacent elbow and carpometacarpal joints. Thirdly, despite the instability of the newly rebuilt wrist, only some patients experienced mild or intermediate pain, which may explain the relatively high satisfaction rate among our patients.
Oncologic Outcomes
There was only one local recurrence in our series of 12 patients, which is consistent with or lower than other reported local recurrence rates. Although many authors have reported no local recurrence in small series, Saini et al. and Chadha et al. reported one recurrence in 12 and 9 patients, respectively8, 9, 13, 15, 39, and Murray and Schlafly reported a recurrence rate of 27.7% in 18 patients12. Compared with this last result, our relatively lower recurrence rate is likely attributable to the relatively short duration of follow‐up: our mean follow‐up was 3.5 years, whereas that of Murray's was 7.1 years. Of note, Balke et al. concluded that recurrent GCT should be considered serious because 10.5% of patients with recurrence develop pulmonary metastases40. Therefore, it is important to achieve a safe margin and use adjuvant therapy if possible to reduce the likelihood of local recurrence and distant metastasis6, 41, 42.
Additionally, one patient in our study developed lung metastases approximately 32 months postoperatively. The reported incidence of lung metastases varies between 1% and 9.1%43, 44, 45. Surgical excision of lung metastases has been widely accepted as the treatment of choice and achieves with excellent long‐term survival45, 46. Interestingly, in our series we treated the lung metastases with gamma knife radiotherapy.
Radiological Outcomes
In the current series of 12 cases, there were two palm subluxations of the carpal bone, one dorsal subluxation and one dorsal dislocation, which is similar to radiological outcomes reported by others9, 27, 47, 48. Saini et al. reported 3/12 cases of subluxation, all of which were managed conservatively9. Maruthainar et al. reported 4/13 cases of wrist subluxation47. Saikia et al. also reported 10 cases (n = 24) of subluxation, six of which were asymptomatic48. Additionally, in our study, there were six cases of distal radioulnar joint diastasis and seven of ulnar deviation of the wrist. Both of those two complications have seldom been reported previously, which prevented us from making comparisons with other studies.
Our incidence of radiocarpal arthritis (11/12) and bone resorption (10/11) seems relatively high. Chung et al. reported that seven of 12 patients with Enneking stage II giant cell tumors developed mild arthritis of the wrist and the remaining five patients had subluxation and developed considerable osteoarthritic change27. Such degenerative changes indicate instability of the wrist, which may result from the following. First, as suggested by Zhang and Wu, instability of the wrist may be due to structural instability caused by an incongruity between the articular surfaces of the fibular head and proximal carpal bones49. Second, involved adjacent soft tissues are routinely removed to attain a safe margin in the case of aggressive lesions. Even repaired with ligament, tendon or capsules, the stability of soft tissue is partly impaired.
Interestingly, despite the high incidence of radiological complications, all patients were satisfied with the functional and cosmetic results. Consequently, no further surgeries were required for these complications. We expected from our previous experience that these structural changes might have negative impacts on wrist function. Further research with more cases is required to clarify the relationship between radiological changes and functional outcomes. The resultant data would be helpful for further optimizing this widely used technique.
Limitations
This study has several limitations. First, our study is retrospective and has a small sample size. For one thing, GCT of the distal radius is not common and only patients treated with non‐vascularized proximal fibular grafts were included in the current study. Patients with recurrent lesions at the initial presentation were also excluded. Even through only 12 cases were eventually included in this series, the sample size is relatively large compared with that of similar studies. Second, the approaches to GCT management and patient rehabilitation in the four participating centers have been similar but are not the same. In particular, there was a lack of uniformity in the way K‐wires were utilized to increase the stability of the new wrist joint, which may have somewhat influenced the final result. Third, only the technique of non‐vascularized proximal fibular graft was included in our study; comparison with other reconstructive options was therefore unavailable. Thus, we cannot categorically state that non‐vascularized proximal fibular grafts are a superior means of reconstruction. Based on our experience, we agree with the recommendations of Muramatsu et al. that arthroplasty be preferred for patients who are not involved in heavy manual labor and fibula‐scapho‐lunate arthrodesis for young patients involved in high‐energy activities50.
In summary, though objective outcomes with regard to ROM and radiological evaluation were relatively poor, subjective outcomes such as emotional acceptability and pain control were satisfactory. In conclusion, the results of our multicenter study suggest that after en bloc resection of the distal radius for giant cell tumor, reconstruction with non‐vascularized proximal fibular autograft remains a reasonable option. Further studies are necessary to optimize this technique.
Grant Sources: This work was supported by grants from the Natural Science Foundation of Tianjin (No. 12JCYBJCl6400) and Science and Technology Fund of Tianjin Municipal Bureau of Health (No. 2011KY24).
Disclosure: The authors declare they have no conflicts of interest.
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