Excision of proximal fibular aggressive and malignant tumors: a new classification for surgical guidance

Abstract

Background

Patients with aggressive and malignant tumors of the proximal fibula may require en bloc resection to reduce the recurrence rate. We aimed to analyze the clinical curative effect of the surgical treatment of proximal fibula tumors, and the relationship between a new classification system and functional evaluation of the knee and ankle joint.

Methods

Between July 2010 and February 2022, 30 patients with proximal fibula tumors were treated, of which 27 had primary tumors and three had recurrent tumors. The histologic diagnoses were aggressive osteoblastoma (three patients), ‘active’ osteochondroma (five patients), giant cell tumor of the bone (11 patients), chondrosarcoma (four patients), osteosarcoma (six patients), and metastatic carcinoma (one patient). The surgical methods were divided into four types according to two important anatomical structures—the deep peroneal nerve (DPN) and proximal tibiofibular joint (PTFJ). Brief descriptions of the removal methods are as follows. Type I includes intra-articular resection of the PTFJ and preservation of the DPN. Type II includes the resection of the DPN and intra-articular resection of the PTFJ. Type III includes extra-articular PTFJ resection and preservation of the DPN. Type IV includes extra-articular PTFJ resection and resection of the DPN.

Results

The 30 patients with proximal fibula tumor underwent successful operation. Those who underwent type I and type III procedures had normal ankle function because the DPN was preserved; however, in those who underwent type II and type IV procedures with resection of the DPN, ankle foot orthosis was needed to stabilize the ankle joint because of the resulting drop foot. In those who underwent type I and type II procedures with intra-articular PTFJ resection, the preservation of the lateral collateral ligament, biceps tendon, and popliteal tendon partly protected the structure of the knee joint, leading to postoperative knee joint stability. In those who underwent type III and type IV procedures with extra-articular PTFJ resection, gait abnormalities and knee instability occurred.

Conclusions

The peroneal nerve and PTFJ are adjacent to each other, and resection of proximal fibular tumors is challenging for orthopedic surgeons. The DPN and PTFJ classification can lead to better surgical planning and postoperative functional evaluation. It provides useful information for the standardized treatment of proximal peroneal tumors based on regional anatomy.

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Key findings

• The study proposes a novel surgical classification system for proximal fibular tumor resection, which is anatomically grounded in the tumor’s spatial relationship to two key structures: the proximal tibiofibular joint (PTFJ) and the deep peroneal nerve (DPN).

What is known and what is new?

• For proximal fibular aggressive or malignant tumors, wide resection is essential to achieve local control. Traditional surgical approaches have primarily relied on tumor differentiation for classification.

• The novel surgical classification system depends not only on tumor malignancy grade but also incorporates three critical anatomical determinants: (I) tumor location; (II) tumor dimension; and (III) extent of local tissue invasion.

What is the implication, and what should change now?

• The specific perspective of basing surgical planning and resection extent primarily on the status of two key structures: the PTFJ and the DPN.

• The emphasis that this system specifically guides functional recovery (knee and ankle) post-operatively by dictating the necessary extent of resection relative to these structures.

Introduction

Fibula tumors account for approximately 2.5% of all primary bone tumors. Osteosarcoma, Ewing’s sarcoma, and giant cell tumors of the bone are common types of proximal fibula tumors. There is a close relationship between the peroneal nerve, anterior tibial artery, and the fibular head; therefore, surgical treatment of proximal fibular tumors is challenging (1,2). When aggressive or malignant tumors invade the deep peroneal nerve (DPN) and proximal tibiofibular joint (PTFJ), to reduce local recurrence, both structures must be sacrificed. The sacrifice of the DPN leads to foot drop, and the sacrifice of the PTFJ leads to instability of the lateral compartment of the knee joint (3,4). Although Malawer (3) and Erler et al. (5) described resection techniques for malignant and aggressive benign proximal fibula tumors in 1984 and 2004, respectively, only a few studies have investigated the clinical outcomes of knee and ankle function after different types of resections. This study reviewed the therapeutic outcomes of bone tumors localized in the proximal fibula, which were managed according to a new classification system, aiming to evaluate clinical efficacy and function of the knee and ankle joint after proximal fibula resection. We present this article in accordance with the STROBE reporting checklist (available at https://aoj.amegroups.com/article/view/10.21037/aoj-25-47/rc).

Methods

The records of 30 patients with aggressive and malignant tumors of the proximal fibula who underwent proximal fibular resection by the author between July 2010 and February 2022 were reviewed. Lesions that occurred in the fibular shaft or distal fibula were excluded. The indications for the classification are shown in Figure 1. The histological diagnoses were aggressive osteoblastoma (three patients), ‘active’ osteochondroma (active osteochondroma was an enlarged lesion with a cartilage cap of >10-mm thickness, five patients), giant cell tumor of the bone (11 patients), chondrosarcoma (four patients), osteosarcoma (six patients), and metastatic carcinoma (one patient). Radiography, magnetic resonance imaging (MRI), and staging with computed tomography (CT) of the chest were performed preoperatively. There were 27 primary cases and three cases of recurrence. Surgical excision was based on the DPN and PTFJ classification. Brief descriptions of the resections are as follows. Type I includes intra-articular resection of the PTFJ and preservation of the DPN (Figure 2A, images A1-A4). Type II includes resection of the DPN and intra-articular resection of the PTFJ (Figure 2B, images B1-B4). Type III includes extra-articular resection of the PTFJ and preservation of the DPN (Figure 2C, images C1-C4). Type IV includes extra-articular resection of the PTFJ and DPN (Figure 2D, images D1-D4). Patients with osteosarcoma received chemotherapy according to established protocols. The follow-up ranged between 6 and 144 months (average 74.2 months). The clinical data of patients, such as sex, age, disease type, surgical treatment, limb function, oncology follow-up (recurrence and metastasis), and preoperative and postoperative visual analog scale (VAS) pain scores, were collected and analyzed. The information is presented in Table 1. The data of those lost to follow up were recorded, including the last follow-up time and status. During outpatient follow-up, standing position radiography and CT were performed, and patients with malignant tumors underwent CT of the lung at the same time. According to the Musculoskeletal Tumor Society (MSTS) (6), patients were assessed based on the postoperative functional evaluation index, including pain, function, psychological support, walking, and gait (six items with 5 points each—maximum 30 points). The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of the Beijing Jishuitan Hospital Guizhou Hospital (No. KT20100713015) and informed consent was taken from all the patients.

Figure 1.

Tumor types in patients with proximal fibula resection.

Figure 2.

Surgical management and imaging findings in four patients with proximal fibular tumors. (A) A 19-year-old patient with a giant cell tumor of the proximal fibula. A wide resection of the proximal fibula (type I) was necessary. (A1) Preoperative radiograph showing osteolytic-osteoblastic lesion. (A2) CT showing the proximal fibula tumor. (A3) Intraoperative picture showing that the peroneal nerve was retained and the lateral tibial wall was intact. (A4) Postoperative specimens. (B) A 34-year-old patient with a giant cell tumor of the proximal fibula. A wide resection of the proximal fibula (type II) was necessary. (B1) Preoperative radiograph showing osteolytic-osteoblastic lesion. (B2) CT showing soft tissue mass in the proximal fibula with a circular calcification on the edge. (B3) Intraoperative picture showing resection of the deep peroneal nerve and intra-articular resection of proximal tibiofibular joint. (B4) Postoperative specimens. (C) A 25-year-old patient with a giant cell tumor of the proximal fibula. A wide resection of the proximal fibula (type III) was necessary. (C1) Preoperative radiograph showing osteolytic-osteoblastic lesion. (C2) CT showing the proximal fibula tumor. (C3) Intraoperative picture showing that the peroneal nerve was retained and the proximal tibiofibular joint was excised extra-articularly. (C4) Postoperative specimens. (D) A 32-year-old patient with an osteosarcoma of the proximal fibula. A wide resection of the proximal fibula (type IV) was necessary. (D1) Postoperative radiograph findings 1 year later with a soft tissue mass around the proximal fibula. (D2) T1W1 examination showing recurrence of peroneal stump tumor. (D3) T1W1 examination showing tumor invasion of the common peroneal nerve and the anterior tibial muscle group. (D4) Postoperative specimens. CT, computed tomography; T1W1, T1-weighted imaging.

Table 1. Details of patients after surgery.

Case	Sex	Age (years)	Disease	Resection type	MSTS score	Tumour recurrence	Mortality
1	F	56	“Active” osteochondroma	Type I	30	No	N/A
2	F	31	Aggressive osteoblastoma	Type I	30	No	N/A
3	F	51	“Active” osteochondroma	Type I	30	No	N/A
4	F	19	Giant cell tumor of bone	Type I	30	No	N/A
5	M	61	“Active” osteochondroma	Type I	30	No	N/A
6	F	34	Giant cell tumor of bone	Type I	28	No	N/A
7	F	16	Aggressive osteoblastoma	Type I	29	No	N/A
8	F	63	“Active” osteochondroma	Type I	29	No	N/A
9	F	21	Aggressive osteoblastoma	Type I	30	No	N/A
10	M	23	“Active” osteochondroma	Type I	29	No	N/A
11	F	37	Giant cell tumor of bone	Type I	30	No	N/A
12	F	32	Giant cell tumor of bone	Type I	28	No	N/A
13	M	50	Chondrosarcoma	Type II	24	No	N/A
14	F	54	Chondrosarcoma	Type II	23	No	N/A
15	M	34	Giant cell tumor of bone	Type II	25	No	N/A
16	F	56	Giant cell tumor of bone	Type II	24	No	N/A
17	F	24	Osteosarcoma	Type II	23	No	N/A
18	M	60	Giant cell tumor of bone	Type II	26	No	N/A
19	F	10	Osteosarcoma	Type II	25	No	N/A
20	M	39	Giant cell tumor of bone	Type III	28	No	N/A
21	F	25	Giant cell tumor of bone	Type III	27	No	N/A
22	M	43	Giant cell tumor of bone	Type III	28	No	N/A
23	M	18	Osteosarcoma	Type III	27	No	N/A
24	F	23	Osteosarcoma	Type III	28	Yes—at 2 years	At 3 years
25	F	35	Giant cell tumor of bone	Type IV	25	No	N/A
26	F	49	Metastatic carcinoma	Type IV	26	No	N/A
27	M	32	Osteosarcoma	Type IV	22	No	N/A
28	M	17	Osteosarcoma	Type IV	25	Yes—at 2 years	At 3 years
29	F	37	Chondrosarcoma	Type IV	24	No	N/A
30	F	38	Chondrosarcoma	Type IV	23	No	N/A

F, female; M, male; MSTS, Musculoskeletal Tumor Society; N/A, not applicable.

Results

Regarding sex distribution, there were 20 female and 10 male patients. There were 19 aggressive and 11 malignant bone tumors. The patients’ ages ranged between 10 and 63 years, with a mean of 36.2 years. There were 12 cases of type I, seven of type II, five of type III, and six of type IV. In the initial surgery, 19 patients (type I and type II) underwent intra-articular resection of the PTFJ. The lateral collateral ligament and lateral-head tendon of the biceps femoris were separated from the fibular head and reconnected to the lateral tibial wall with sutures. The stable structure around the knee joint was preserved, the knee joint stability was good, and no obvious pain was reported. One of the 12 type I patients (case 2) had decreased dorsal extensor strength after surgery, but the DPN was preserved, and the muscle strength fully recovered 3 weeks after surgery. The seven type II patients had foot drop due to DPN resection, but three of the seven patients (cases 15, 18, and 19) had no obvious abnormal gait when walking on high heels. The other four type II patients (cases 13, 14, 16, and 17) wore ankle foot orthosis (AFO) for a long time. Among the 30 patients, 11 (type III and type IV) underwent extraarticular resection of the PTFJ, and the lateral ligament complex was connected to the tibia with a simple suture. Two of the five type III patients (cases 22 and 24) complained of slight pain on the lateral side of the knee joint when walking for overly long periods, while the remaining three of the five patients (cases 20, 21, and 23) complained of poor knee stability during running. The six type IV patients needed to wear an AFO for a long time because of the resection of the DPN, and functional recovery of the affected limb was evaluated according to the MSTS score. The score range of type I, II, III, and IV patients was 28–30, 23–26, 27–28, and 22–26, respectively (Figure 3). The preoperative and postoperative VAS scores were 3.43±1.94 and 0.67±0.64, respectively. Postoperative pain was completely relieved in 25 patients (VAS =0) and was mild in the remaining patients (VAS ≤2). Nine of the 11 patients with malignant bone tumors survived for 6–144 months without local recurrence or distant metastasis. The median survival time was 71.5 months. Two patients with osteosarcoma had pulmonary metastasis 24 months after the surgery and were treated with chemotherapy. Two patients (cases 24 and 28) died of multiple metastases 38 and 40 months after surgery, respectively. The patient data are summarized in Table 2.

Figure 3.

Postoperative MSTS function scores of patients with regard to the different surgical methods. MSTS, Musculoskeletal Tumor Society.

Table 2. Classification system for the resection of the proximal fibula.

	N0= preserving the peroneal nerve	N1= resection of the deep peroneal nerve
T0= intraarticular resection of the proximal fibula	I	II
T1= extraarticular resection of the tibiofibular joint	III	IV

N, resection of the peroneal nerve; T, resection of the tibiofibular joint.

Discussion

The proximal fibula is a rare site of primary or metastatic bone tumors. Complete resection is the most effective treatment for aggressive or malignant bone tumors. However, owing to the complex anatomical structure of the proximal fibula, knee instability, tumor recurrence, peroneal nerve palsy, arterial dysfunction, and other complications may occur after tumor resection. Therefore, it is important to choose a reasonable surgical method to improve the prognosis of patients.

Two important anatomical structures, the PTFJ and DPN, make the management of extraosseous proximal fibula tumors challenging (7). The PTFJ plays an important role in maintaining the stability of the knee joint by transferring the stress load between the knee joint and ankle joint, acting as the attachment point of the muscle and reducing the bending movement of the outside of the tibia (8-10). If the PTFJ is removed during surgery, gait is affected to some extent (11). The DPN is one of the branches of the common peroneal nerve, which innervates the tibialis anterior, extensor digitorum longus, extensor longus, and dorsalis pedis. The removal of the DPN may lead to serious complications, such as high gait, foot drooping, and gait instability (12).

Malawer (3) summarized two types of resection according to benign and malignant tumors: type I resection is extensive but conservative; type II resection is also wide but is more invasive. Erler et al. (5) described two more detailed types of resection according to tumor volume and whether the joint was invaded by the tumor on MRI; they noted that if the tumor volume is >250 mL, the DPN must be removed to obtain a safe surgical margin. However, this method is mostly suitable for tumors with high recurrence rates. For osteochondroma, even if the volume is >250 mL, the tumor can be removed with preservation of the DPN, but the peroneal nerve should be properly released (13). These suggest that no single treatment method can be used in relation to the preoperative planning and postoperative prediction of knee and ankle function. Our classification system considers two important anatomical structures—the DPN and PTFJ. Its advantage is that it can be used to clearly formulate the surgical plan and effectively evaluate the functional changes in the knee and ankle joints after surgery. In addition, this classification can make it easier for patients and their families to understand their own disease characteristics and prognosis. In this classification, the extent of tumor resection also depends on tumor size, degree of tumor differentiation, local recurrence rate, and other major adjacent anatomical structures.

If the PTFJ is clear on CT, intra-articular excision is required. Therefore, it is necessary to separate the lateral collateral ligament and biceps femoris muscle, which stabilize the knee, from the head of the fibula before removing the proximal end of the fibula. The lateral collateral ligament is a knee joint ligament that limits excessive posterior extension and external rotation of the knee joint (14). Einoder and Choong did not perform any reconstruction of the external collateral ligament after resection of the proximal fibula tumor, and the knee joint remained stable during the 4-year follow-up; however, two patients were found with a 1-cm widened joint space in the recheck radiography (15), which led to osteoarthritis in the subsequent long-term follow-up (8). Therefore, we believe that reconstruction of the lateral collateral ligament is an effective measure to prevent knee osteoarthritis for young patients who need intra-articular resection. In our series, the lateral collateral ligament (LCL) and biceps were separated from the fibular head and reconnected to the lateral wall of the tibia with sutures. None of the patients complained of knee instability or valgus instability during the follow-up (type I, type II). If the PTFJ cannot be saved, extra-articular PTFJ resection is required to reach a safe surgical boundary. However, the need for subperiosteal dissection for tumors on the tibial side (16,17) or lateral tibial wall resection (18) remains controversial. To reduce the local recurrence rate, we chose to resect the lateral wall of the tibia, and no patient experienced recurrence after surgery. Gait abnormalities and knee instability occurred after extra-articular PTFJ resection. Draganich et al. proposed that patients with tumors in the proximal fibula may have abnormal gait and instability of the knee joint after extraarticular PTFJ resection (8). Therefore, it is suggested that the remaining lateral collateral ligament and biceps tendon should be properly reconnected to the tibial metaphysis to maintain the stability of the knee joint. In our study series, two patients who had a type III (extra-articular PTFJ resection) experienced mild pain on the lateral side of the knee joint when they walked for long periods. Three patients complained of poor knee stability during running. MRI can be used to check whether the DPN is retainable. If a malignant tumor infiltrates the nerve, the nerve must be resected to obtain adequate surgical margins and should not be preserved. In cases where the tumor is only superficially adherent to the peroneal nerve, epineurectomy is an acceptable approach to achieve wide resection. Patients need to wear AFO to perform their normal activities as in our series (type II and type IV).

The functional results of type I and III patients were significantly better than those of type II and IV patients. This is not surprising, because the DPN was removed in type II and IV patients. The stability of the knee joint in type III and IV patients was significantly worse than that of type I and II patients, because the PTFJ was removed extra-articularly in type III and IV patients, and the stable reconstruction attachment point was lost. The advantage of this type of classification is that the operation plan can be simply and clearly formulated before the surgery, and patients can have a better understanding of their disease recovery during preoperative discussions between doctors and patients. After surgery, effective rehabilitation exercises and protective measures can be formulated according to the type of patient.

However, this study has several limitations. Its retrospective design, limited sample size from a single institution, and broad age distribution resulted in varied baseline activity levels among participants. Although this heterogeneity reflects clinical reality, it introduces uncontrollable variability that may affect the interpretation of functional outcomes. These limitations have been explicitly acknowledged in the manuscript. Further validation through larger, multi-center trials with stratified analyses based on age and activity level is warranted.

Conclusions

We suggest that satisfactory clinical results can be obtained by selecting four different resection techniques. In addition, resection of the DPN can also provide a safe surgical boundary in some aggressive tumors or malignant tumors with soft tissue components, which will require reconstruction of the lateral stability of the knee. However, gait abnormalities and knee instability occurred after extra-articular PTFJ resection in our series. This study provides a different perspective to the orthopedic surgeon for the resection of proximal fibular tumors based on the two important anatomical structures around the knee joint, PTFJ and the DPN. Each procedure permits limb salvage, and they are differentiated by the extent of tissue resection. It is not only simple and convenient but can also be used to guide the recovery of knee and ankle joint function after surgery.

Supplementary

The article’s supplementary files as

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of the Beijing Jishuitan Hospital Guizhou Hospital (No. KT20100713015) and informed consent was taken from all the patients.

Data Sharing Statement

Available at https://aoj.amegroups.com/article/view/10.21037/aoj-25-47/dss

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DOI: 10.21037/aoj-25-47