The Journal of Bone & Joint Surgery

The Journal of Bone & Joint Surgery, Volume 94, Issue 5

Scientific Articles | March 07, 2012

Giant Cell Tumor of the Extremity: Retrospective Analysis of 621 Chinese Patients from One Institution

Xiaohui Niu, MD¹; Qing Zhang, MD¹; Lin Hao, MD¹; Yi Ding, MD¹; Yuan Li, MD¹; Hairong Xu, MD¹; Weifeng Liu, MD¹

¹ Department of Orthopedic Oncology Surgery, Beijing Ji Shui Tan Hospital, Peking University, 31 Xinjiekou East Street, Xicheng District, Beijing 100035, China. Email address for X. Niu: niuxiaohui@263.net

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Investigation performed at the Department of Orthopedic Oncology Surgery, Beijing Ji Shui Tan Hospital, Peking University, Beijing, China

Disclosure: None of the authors received payments or services, either directly or indirectly (i.e., via his or her institution), from a third party in support of any aspect of this work. None of the authors, or their institution(s), have had any financial relationship, in the thirty-six months prior to submission of this work, with any entity in the biomedical arena that could be perceived to influence or have the potential to influence what is written in this work. Also, no author has had any other relationships, or has engaged in any other activities, that could be perceived to influence or have the potential to influence what is written in this work. The complete Disclosures of Potential Conflicts of Interest submitted by authors are always provided with the online version of the article.

J Bone Joint Surg Am, 2012 Mar 07;94(5):461-467. doi: 10.2106/JBJS.J.01922

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Abstract

Background:

There are no recent reports of giant cell tumors of bone in a large series of Chinese people. The present study was designed to review the epidemiological characteristics and outcomes of surgical management in a large series of Chinese patients with giant cell tumor of an extremity, treated at a single institution.

Methods:

The records and images of 621 patients in whom a benign giant cell tumor in an extremity was treated between 1989 and 2009 were reviewed retrospectively. There were 359 male and 262 female patients. The mean age at diagnosis was 31.4 years (range, eleven to seventy-one years). Sixty-six percent of the giant cell tumors were localized around the knee. Surgical treatments primarily included curettage, extensive curettage, and resection. The median duration of follow-up was forty-nine months (range, eighteen to 256 months).

Results:

Giant cell tumor accounted for 13.7% of all primary bone tumors treated at our institution. Multivariate Cox regression analysis indicated that the only variable that contributed to recurrence-free survival was the type of surgical treatment. The local recurrence rate after extensive curettage was 8.6%, which was significantly lower than the 56.1% recurrence rate after curettage alone. Bone-grafting did not affect local tumor control after extensive curettage; the local recurrence rate was 11.1% if bone graft was used. Recurrent giant cell tumor can be treated by further curettage or resection, with acceptable re-recurrence rates of 6.7% and 9.3% respectively. The Musculoskeletal Tumor Society Score for patients treated with extensive curettage was 92.6%, which was significantly higher than that for patients treated with resection. Twenty-one (3.4%) of the 621 patients developed benign pulmonary metastasis, with a favorable outcome, and three patients presented with multifocal giant cell tumors.

Conclusions:

The incidence of giant cell tumor in the Chinese population may be higher than that in Western countries, and it has a male predilection. The results of the present study suggest that extensive curettage provides favorable local control and satisfactory functional outcomes.

Level of Evidence:

Therapeutic Level III. See Instructions for Authors for a complete description of levels of evidence.

Figures in this Article

Introduction

Introduction | Materials and Methods | Results | Discussion | Appendix

Giant cell tumor of bone is defined as a primary intramedullary bone tumor composed of mononucleated cells and osteoclast-like multinucleated giant cells and presenting as a locally aggressive lesion with unpredictable behavior¹. It accounts for 20% of all benign tumors and 5% of primary bone tumors². However, the reported incidence in some Asian countries may account for 20% of all musculoskeletal tumors^3,4.

The ideal treatment for giant cell tumor remains controversial. Although almost 100% local control can be achieved with en bloc resection⁵, limb function is usually compromised because of the periarticular location of most giant cell tumors⁶. Intralesional excision with curettage is the standard method of treatment, but that has been associated with local recurrence rates ranging from 10% to 40%^7-12. As a result, topical adjuvant agents, such as hydrogen peroxide, phenol, and alcohol, have been used to decrease the recurrence rates. However, a recent meta-analysis demonstrated that local control was not improved with use of adjuvants¹³. The purpose of our study was to report the results in Chinese patients with a giant cell tumor in an extremity who were treated at one institution. Our hypothesis was that the epidemiology of giant cell tumor in Chinese people differs from that in other populations and aggressive curettage with high-speed burring can provide satisfactory local control and functional outcomes.

Materials and Methods

Introduction | Materials and Methods | Results | Discussion | Appendix

This was a retrospective study based on a review of patients’ records and imaging data. Six hundred and twenty-one patients with a giant cell tumor of an extremity were treated at the Department of Orthopedic Oncology Surgery at our institution between 1989 and 2009 (Fig. 1). All lesions were histologically confirmed as benign giant cell tumors. Of the 621 patients, 395 met the criteria for evaluation of the treatment; these criteria included at least one definitive surgical procedure done in our institution and a minimum duration of follow-up of eighteen months after this surgery. Patients who were referred from other hospitals not as a result of local recurrence but because of specific complications were excluded.

Fig. 1

Series cases map for the original 621 cases of giant cell tumor (GCT). MSTS = Musculoskeletal Tumor Society.

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This series included 507 cases (81.6%) located in the lower limb and 114 (18.4%), in the upper limb. There were 359 male and 262 female patients, a ratio of 1.4:1 (see Appendix). The mean age at the time of the first diagnosis was 31.7 years (range, eleven to sixty-seven years) for male patients, 30.9 years (range, thirteen to seventy-one years) for female patients, and 31.4 years (range, eleven to seventy-one years) overall. Sixty-six percent of the giant cell tumors were located around the knee (210 were in the distal part of the femur; 180, in the proximal part of the tibia; eighteen, in the proximal part of the fibula ; and two, in the patella), 10.6%, were in the proximal part of the femur (n = 66), 8.2% were in the distal part of the radius (n = 51), and 7.4% were in the proximal part of the humerus (n = 46). The rest (n = 48) were in other locations (Fig. 2).

Fig. 2

Anatomical distribution of the 621 giant cell tumors. The majority of lesions affected the meta-epiphyseal region of the long bones, especially around the knee joint.

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Treatment analysis was based on 395 patients with at least eighteen months of follow-up (Fig. 1). Preoperative imaging included radiographs of the lesion, computed tomography (CT), magnetic resonance imaging (MRI), nuclear scintigraphy, a chest radiograph, and a chest CT scan. The giant cell tumor was graded according to the Campanacci staging system¹.

Treatment primarily included curettage, extensive curettage, or resection. Curettage was intralesional and was done with a series of curets of various sizes to remove visible tumor. Extensive curettage was carried out as follows. First, a lateral or medial approach was chosen, depending on the more affected side. One cortical window was made to access the entire tumor area to avoid having to use the curet under overhanging shelves or ridges of bone. Generally, the length of the window should be 10 mm larger than the tumor in the longitudinal direction and the width should be at least one-fourth to one-fifth larger than the perimeter in cross section. Part of the soft-tissue capsule over the tumor cortex should be removed, and the thickness of the removed tissue should be 5 mm. Second, the tumor was removed with curets of various sizes. Third, the residual cavity was burred with a high-speed burr at least 10 mm into the normal cancellous bone and/or 1 mm into the normal cortical bone, except for the articular cartilage aspect. On the articular side, the subchondral bone was maintained when there was >10 mm of bone. If <10 mm of bone remained, not all subchondral bone (only the most affected) was removed. Fourth, the curettage fields were washed with pulse irrigation. A dental mirror combined with a head lamp helped the surgeon to identify and access small pockets of residual lesions, which may result in recurrence. After extensive curettage, the cavity was filled with bone cement if the integrity of the subchondral bone was not damaged. Otherwise, the subchondral bone area was packed with bone graft of about 10 mm in thickness and the remaining cavity was filled with bone cement. Bone graft could be allograft, autogenous graft, or a bone substitute. At least one adjuvant, such as phenol, alcohol, or bone cement, was used in curettage or extensive curettage procedures. Materials for reconstructing the cavity after curettage were mainly grouped as follows: cement packing alone, cement packing with a subchondral bone graft, and bone graft alone. The choice of reconstruction was at the discretion of the treating surgeons and also depended on the patient’s age.

Indications for en bloc resection included a large tumor with soft-tissue extension, reconstruction not possible after curettage, pathological fracture with joint involvement, repeated recurrence, and tumor in an expendable bone (the proximal part of the fibula or distal part of the ulna). Prostheses, segmental allografts, allograft-prosthesis composites, or devitalized (by 95% alcohol for thirty minutes) host tumor bone shells were used to reconstruct the bone defects after resection.

Of the 621 patients, 395 (63.6%) were followed for at least eighteen months and the remaining 226 (36.4%) were lost to follow-up. The follow-up consisted of clinic visits or telephone interview. Of the 395 patients, 306 (77.5%) were seen in our clinic, with a physician performing an examination and radiographs made at each visit. The remaining eighty-nine patients (22.5%) were followed with a telephone interview, which was conducted after the primary surgeons reviewed radiographs made at local hospitals. The patients were followed every three months for the first two years after the surgery, every six months until the fifth year, and every year until the tenth year. The telephone interview was allowed only after five years of follow-up. At each follow-up interval, radiographs of the involved area and a CT scan of the chest were obtained. The Musculoskeletal Tumor Society Score¹⁴ was used to assess functional results. The median duration of follow-up was forty-nine months (range, eighteen to 256 months).

Statistical Methods

Statistical analysis was done with SPSS software (version 16.0; SPSS, Chicago, Illinois). Continuous variables such as age and time of follow-up were expressed as the mean, median, and standard deviation of the mean. Categorical variables such as the local recurrence rate and pulmonary metastasis rate were expressed as percentages. One-way analysis of variance (ANOVA) was used to determine differences in functional results among the different surgical procedures. Chi-square analysis was performed to evaluate the difference in various percentages. Kaplan-Meier survival analysis was performed in the univariate analysis. Cox survival regression analysis with the Wald method was performed as a multivariate analysis to determine the best prognostic factors for recurrence. A p value of 0.05 was considered significant.

Source of Funding

No funding was received in support of this research.

Results

Introduction | Materials and Methods | Results | Discussion | Appendix

There were 283 patients who received their initial surgical treatment in our hospital (defined as those with a primary giant cell tumor) and 112 who were referred from other hospitals because of local recurrence (defined as those with a recurrent giant cell tumor). Of the patients with a primary giant cell tumor, 126 had resection and all but twelve of them had reconstruction with a massive bone graft, a prosthesis, or an allograft-prosthesis composite. Of the twelve cases treated with resection only, eight were in the fibula and one each was in the distal part of the ulna, the talus, the proximal part of the humerus, and the distal part of the radius. One hundred and sixteen patients were treated with extensive curettage with filling of the defect with bone cement alone (fifty-nine, 50.9%), bone-chip grafting alone (twenty-six, 22.4%), or bone cement in combination with a subchondral bone graft (thirty-one, 26.7%). Forty-one patients were managed with simple curettage with filling of the defect with bone cement alone (nine, 22.0%), bone-chip grafting alone (thirty-one, 75.6%), or no filling (one, 2.4%).

Local Recurrence of Primary Giant Cell Tumor

Thirty-five (12.4%) of the 283 patients with a primary giant cell tumor developed a local recurrence after a median of nineteen months (range, one to eighty-eight months) (Fig. 3). The local recurrence rate varied depending on the type of surgery. The highest recurrence rate of 56.1% (twenty-three of forty-one) was in the curettage alone group, followed by 8.6% (ten of 116) in the extensive curettage group, and 1.6% (two of 126) in the resection group. The difference between curettage and the other two groups was significant (p = 0.000) (Fig. 4). In the group with extensive curettage, the local recurrence rate was 11.1% (three of twenty-seven) in patients treated with bone-graft filling, 3.3% (one of thirty) in those treated with bone cement combined with bone graft, and 10.2% (six of fifty-nine) in those treated with bone cement alone; these differences were not significant (p = 0.521).

Fig. 3

Kaplan-Meier curve of the cumulative survival, with local recurrence as the end point, based on 283 cases.

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Fig. 4

Kaplan-Meier curve of the cumulative survival, with local recurrence as the end point, according to the type of surgery, based on 283 cases.

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Local recurrence occurred in one patient (25.0%) with a Campanacci grade of 1, twenty-eight (14.8%) with a grade of 2, and four (4.6%) with a grade of 3. The difference of local recurrence between grades 2 and 3 was significant (p = 0.014). The local recurrence rate was 13.8% (thirteen of ninety-four) in the distal part of the femur, 11.8% (nine of seventy-six) in the proximal part of the tibia, 20.5% (eight of thirty-nine) in the proximal part of the femur, 7.1% (two of twenty-eight) in the distal part of the radius, 5% (one of twenty) in the proximal part of the humerus, and 7.7% (two of twenty-six) in other sites, without any significant difference among sites.

Sex, age, and a pathological fracture in the involved location were not found to have a significant effect on local recurrence. Multivariate Cox regression analysis with the forward Wald method, with consideration of sex, age, tumor grade, tumor site, type of surgery, and pathological fracture at the involved site, indicated that the only variable contributing to recurrence-free survival was the type of surgical procedure (Table I).

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TABLE I Results of Multivariate Cox Analysis*

	Odds Ratio (95% Confidence Interval)	Wald Statistic
Resection	1
Extensive curettage	6.3 (1.4-28.7)	P = 0.018
Curettage	43.7 (10.2-186.7)	P = 0.000

*Regression analysis with the forward Wald method indicated that the only variable that contributed to recurrence-free survival was the type of surgery. Patients treated with curettage had a higher local recurrence rate compared with the other two groups.

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TABLE I Results of Multivariate Cox Analysis*

	Odds Ratio (95% Confidence Interval)	Wald Statistic
Resection	1
Extensive curettage	6.3 (1.4-28.7)	P = 0.018
Curettage	43.7 (10.2-186.7)	P = 0.000

When tumors treated before and after 2001 were defined as old and new cases, respectively, we found that the local recurrence rate for old cases (50.5% of which were treated with resection) was 27.5%, while the new cases (41.7% of which were treated with resection) had a significant lower recurrence rate of 5.2% (p = 0.000).

Treatment of Recurrent Giant Cell Tumor

There were 147 patients with recurrent giant cell tumor, including thirty-five who had been primarily treated in our hospital and 112 who had been referred from other hospitals (Fig. 1). All patients received additional surgery except for one who refused it. The rate of local re-recurrence was 6.7% (four patients) in the sixty patients treated with repeat curettage and 9.3% (eight patients) in the eighty-six treated with resection. The overall rate of local re-recurrence (8.2%; twelve of 146) was not higher than the first-recurrence rate (12.4%) (p = 0.192). However, eighty-six patients (58.9%) with recurrence had been treated with tumor resection and reconstruction with a prosthesis or segmental allograft; this rate was significantly higher than the rate (44.5%) of first surgical procedures done with this technique (p = 0.005).

Pulmonary Metastases of Giant Cell Tumor

The overall pulmonary metastasis rate of giant cell tumor was 3.4% (twenty-one of 621). Two of the twenty-one cases were histologically confirmed as benign pulmonary metastases, with the pulmonary nodules newly formed and >10 mm in diameter. The remaining nineteen patients were diagnosed on the basis of a CT scan. Thirteen (61.9%) of the twenty-one patients with pulmonary metastasis developed local recurrence. The rate of pulmonary metastasis was 8.6% (three of thirty-five) in the patients with recurrence and 2.4% (six of 248) in those without recurrence. The mean interval between the diagnosis of giant cell tumor and pulmonary metastasis was 39.6 months (range, zero to 167 months). The pulmonary metastases were treated with bisphosphonates in four cases and chemotherapy (ifosfamide and Adriamycin [doxorubicin]) in one case. After a mean duration of follow-up of 75.7 months (range, twenty-three to 213 months), one patient had developed scalp metastasis, two patients had died of the disease without a pulmonary tissue diagnosis, and the remaining eighteen patients had experienced stable pulmonary disease without specific treatment. One patient developed heart metastasis without pulmonary involvement and died of the metastasis¹⁵.

Multifocal Giant Cell Tumor

The rate of multifocal giant cell tumor in the series was 0.48% (three of 621). One patient, a fifteen-year-old girl, presented with synchronous involvement of the proximal parts of the tibia and femur. Another patient, a seventeen-year-old boy, developed metachronous involvement of the proximal part of the femur followed by the proximal part of the tibia. The third patient, a thirty-seven-year-old woman, had metachronous involvement of the distal part of the femur followed by the proximal part of the femur of the same limb. The treatment for all three cases was surgery at all involved locations followed by administration of bisphosphonates. At the time of final follow-up, two patients were free of disease (at twenty-nine and forty-nine months after the surgery, respectively) and one patient had pulmonary metastasis.

Functional Outcomes

Functional results were available for 197 patients, including five with curettage, eighty-five with aggressive curettage, and 107 with en bloc resection (Fig. 1). Worse function was observed after resection. The mean Musculoskeletal Tumor Society Score (and standard deviation) was 88.9% ± 11.4% overall, 94.7% ± 5.6% for those treated with curettage, 92.6% ± 8.2% for those treated with extensive curettage, and 85.6% ± 12.7% for those treated with resection. One-way ANOVA suggested a significant difference in functional outcome among the three types of surgery. Furthermore, the pairwise post hoc test with least significant difference revealed a significant difference (p = 0.000) between resection and extensive curettage but not between resection and curettage (p = 0.071) or between curettage and extensive curettage (p = 0.678) (Fig. 5).

Fig. 5

Functional results according to the type of surgery with use of the percentage Musculoskeletal Tumor Society (MSTS) Score (30 points = 100%).

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Discussion

Introduction | Materials and Methods | Results | Discussion | Appendix

Giant cell tumor of bone, although one of the most common primary musculoskeletal tumors, continues to be one of the most controversial and discussed bone tumors^16-19. Its incidence is debatable as it has varied in different series^{1-3,8,9,20-29} (see Appendix). The frequently cited incidence (i.e., that it accounts for 5% to 7% of all primary bone tumors) is based on large series in the United States^2,20. The incidence reported for the Asian population (>10%) has usually been higher than those for Western countries except for Sweden (10.8%)²⁶. The highest reported incidence was 30.3% for the population of south India²⁸, while western India showed an incidence of 6.3%²³. According to the “three great races” of Caucasoid, Negroid, and Mongoloid³⁰, south India and western India was mostly inhabited by people of Negroid race and Caucasian race, respectively. The 621 patients described in our study, together with 193 with a giant cell tumor in a location other than an extremity, were all Chinese and belonged to the Mongoloid race. Within the same period of time, 5942 patients with primary bone tumors of all types were admitted to our institution, and the estimated incidence of giant cell tumor was 13.7% (814 of 5942). This higher incidence in the Mongoloid race has been shown in other large series from China^3,24. However, the Japanese people, who belong to the Mongoloid race, have shown low incidences of 2.1% and 7.4%^22,27. Most series from the United States have shown a female predominance, with a male/female ratio of about 0.8^2,9,20,25, whereas cases from Italy and Sweden have shown no sex predilection^1,8,21,26. Our series, however, together with other reports on Asian patients, demonstrated significant male predominance, with ratios ranging from 1.26 to 1.77^3,23,27-29. We believe that giant cell tumor in the Mongoloid race has a male predominance, while there is a female predominance in Caucasians.

In this series, we confirmed that giant cell tumors are more likely to occur in patients between twenty and forty years of age and favor the metaphyses of bones around the knee. Nonetheless, the most frequent location following the knee joint (the distal part of the femur and the proximal part of the tibia) was not the distal part of the radius as reported in most series^{21,23,26,28,31}, but the proximal part of the femur.

Many authors consider the prognosis to be unpredictable as most giant cell tumors behave benignly, some are locally aggressive, and occasionally tumors are malignant^{1,21,25,32-34}. The current principles for selection of surgical treatment are based on retrospective case series^2,21,35,36. Some authors reported a recurrence rate of 35% to 49%^3,19,37, while others reported a lower rate of 12% to 14%^7,38,39. In our series, the local recurrence rate in patients treated with curettage was 56.1%, but when high-speed burring and related surgical techniques were introduced, the local recurrence rate dramatically decreased to 8.6%.

Some authors reported that the recurrence rate varied depending on the tumor site^21,31,35. The reported recurrence rate in the distal part of the radius has ranged from 20% to 88.9%^8,9,40,41. Vander Griend and Funderburk⁴² pointed out that giant cell tumors in the distal part of the radius were particularly aggressive. In their series, 74% (seventeen) of twenty-three patients finally received tumor resection and an additional patient underwent amputation due to recurrence. In our series, 86% (twenty-four) of twenty-eight patients with a tumor in the distal part of the radius underwent tumor resection with a marginal or wide margin, and the recurrence rate was only 7% (two of twenty-eight). On the basis of our series, marginal or wide resection is strongly recommended in sites with a high recurrence rate such as the distal part of the radius.

Campanacci et al.⁸ and others²¹ have reported that the tumor grade was not one of the prognostic factors for recurrence. However, various authors have documented an increased rate of local recurrence of grade-3 lesions^31,43-45. Our series differed in that grade 3 was associated with a significantly lower local recurrence rate compared with grade 2. This might be explained by the choice of operation, since 67.8% of the grade-3 and 34.9% of the grade-2 tumors underwent resection. The result may mean that we should perform more aggressive operations on grade-3 giant cell tumors. Use of adjuvants such as phenol and nitrogen after curettage may be of additional benefit by helping to decrease recurrence rates^35,46. According to the literature^12,21,47,48, most cases recur in the first two to three years after surgery. Although 71.4% of the local recurrences in our series occurred within two years after the surgery, two cases recurred after more than five years. We recommend that patients be followed until ten years after the final surgery.

For recurrent giant cell tumor, some authors have suggested resection with a marginal or wide margin followed by reconstruction with a prosthesis or allograft^37,43. Others⁴⁴ have recommended repeated curettage since it results in a cure in 80% to 90% of cases. Balke et al.⁴⁸ reported a re-recurrence rate of 21.7%, with the need for further curettage, with 20.9% of the patients requiring prosthetic replacement. To our knowledge, the re-recurrence rate following repeat curettage in our series (6.7%) was one of the lowest reported.

Although en bloc resection with marginal excision or a wide margin is well known to produce the lowest recurrence rate, it is not always clear that this should be done because of the benign nature of giant cell tumors and the potential difference in functional results between resection and curettage. Previously published articles^{1,8,44,47,49,50} indicated that functional results were not significantly improved when curettage was performed. Our data support the concept that the functional outcomes of curettage are significantly superior to those of resection. Since extensive curettage resulted in satisfactory control of local recurrence and favorable functional outcomes, we recommend treatment with extensive curettage whenever possible.

In our series, the pulmonary metastasis rate associated with giant cell tumor was 3.4% and the distribution of the primary giant cell tumor sites was similar to those in the literature^35,51-56. It has been reported that an increased pulmonary metastasis rate is associated with local recurrence^10,53,54,57. This concept is supported by our data as the pulmonary metastasis rate in patients with recurrent giant cell tumor was higher than that in those without recurrence. In agreement with the literature^35,58,59, approximately 0.5% of the giant cell tumors in our series presented as synchronous or metachronous lesions. Although the courses of the lesions differed, treatment for multifocal giant cell tumor is the same as that for solitary lesions.

We presented the epidemiological characteristics and results of treatment of giant cell tumors of extremities in a large series of Chinese patients. However, the limitations of this study include the retrospective analysis of results over a twenty-year period, patients treated by different surgeons, follow-up data not being available for 36.4% (226) of the 621 patients, and the results being generally confirmatory of those in prior reported series of patients with giant cell tumor.

Appendix

Introduction | Materials and Methods | Results | Discussion | Appendix

A table comparing different series of giant cell tumors and a figure showing the age and sex distribution of extremity giant cell tumor are available with the online version of this article as a data supplement at jbjs.org.

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Topics

limb ; giant cell tumor of bone ; knee region ; retrospective studies

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Xiaohui Niu, Qing Zhang, Lin Hao, Yi Ding, Yuan Li, Hairong Xu, Weifeng Liu; Giant Cell Tumor of the ExtremityRetrospective Analysis of 621 Chinese Patients from One Institution. The Journal of Bone & Joint Surgery. 2012 Mar;94(5):461-467.

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