Aneurysmal bone cysts (ABCs) are rare, destructive,
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1 ORIGINAL ARTICLE A Review of 56 Patients Kerem BazarNr, MD,* Ahmet Pizkin,Þ Berk Güc$lü,þ Yusuf YNldNz,* and Yener SağlNk* Background: Aneurysmal bone cysts (ABCs) are benign lesions that are usually treated with intralesional procedures. The clinical behavior of ABCs is reported to be more aggressive in younger patients, with high recurrence rates after surgical treatment by several authors. The purpose of this study was to review longitudinally the demographic data and outcome of current surgical techniques in children with ABC treated at a single institution and to determine the possible risk factors for recurrence, which may be detected at initial examination, including age, presenting complaint, and radiological characteristics. Methods: The authors performed a retrospective, pediatric populationybased (e16 years) analysis of 56 cases of ABCs with more than 2 years follow-up. The subjects were studied and classified on the basis of their age group (e5, 5Y10, and 910 years of age). The possible risk factors for recurrence were analyzed initially with Student t test and Pearson W 2 test, then a logistic regression analysis model was used for multivariate analysis. Results: Nine patients were younger than 5 years, 17 were between 5 and 10 years old, and 30 were older than 10 years. The most frequent location of the lesion was the humerus (11 cases) followed by proximal femur and fibula. Curettage was the most common treatment modality followed by resection. Recurrence of the lesion occurred in 5 children in the younger age group and in 4 children in the older age group. The difference in persistence or recurrence rates based on age (e5 years) and previous surgery was statistically significant. In addition, we have found no significant implication of physeal contact and size of the lesion on recurrence. Conclusions: The recurrence rates of primary ABC seemed to be higher in younger children. Considering the high cure rates with intralesional procedures even after recurrence, we suggest less aggressive intralesional procedures even in patients with mentioned risk factors; however, the patients family should be informed about the high probability of recurrence. Level of Evidence: Level III (case-control study). Key Words: aneurysmal bone cyst, children, recurrence, physis, capanna (J Pediatr Orthop 2007;27:938Y943) From the *Department of Orthopedics and Traumatology, Ankara University Medicine Faculty, Department of Orthopedics and Traumatology, 19 MayNs University Medicine Faculty, and Department of Orthopedics and Traumatology, Ufuk University Medicine Faculty, Ankara, Turkey. Each author certifies that he or she has no commercial associations (eg, consultancies, stock ownership, equity interest, patent/licensing arrangements, etc) that might pose a conflict of interest in connection with the submitted article. None of the authors received financial support for this study. Reprints: Dr Kerem BazarNr, AÜTF Ibn i Sina Hospital, Orthopedics and Traumatology Department, SamanpazarN, Ankara, Turkey. basarirkerem@yahoo.com. Copyright * 2007 by Lippincott Williams & Wilkins Aneurysmal bone cysts (ABCs) are rare, destructive, nonneoplastic lesions which have the distended appearance of an aneurysm and controversial pathogenesis. 1,2 World Health Organization defined ABC as an expansile osteolytic lesion consisting of blood-filled spaces and channels that are divided by connective tissue septa which may contain osteoid tissue and osteoclastlike giant cells. 3 It accounts for 1% to 6% of all primary bone tumors and occurs primarily in the first and second decades of life. 1,4,5 As regards ABC pathogenesis, some hypothesized that it is a reactive process resulting from a local alteration in hemodynamics resulting in markedly increased venous pressure and development of a dilated vascular bed within the involved bone. 6,7 In contrast, the presence of a chromosomal translocation t(16;17)(q22;p13) as a recurring abnormality and overexpression of insulin-like growth factor I support the hypothesis that primary ABC is a neoplastic lesion. 1,8,9 The majority of ABCs exist as a primary bone lesion; however, it may occur secondary to other osseous conditions, including giant cell tumor, unicameral bone cyst, and chondroblastoma. 10 De novo ABC is more common in children, whereas pre-existing pathological conditions may account for more than 50% of reported adult cases. 1,11,12 Although ABC is completely benign, this expansile and osteolytic lesion may lead to a pathological fracture. 1,12,13 Thus, intralesional procedures, such as curettage with or without the use of burr, bone marrow injection, or bone grafting, are the most commonly used treatment options, and resection is primarily used in expandable bones. 13,14 Recurrence is most often seen within 24 months following the original treatment 13,15 and ranges from 10% to 59% after different surgical removal techniques. 11,13,15,16 In 1970, Biesecker et al 17 reported a trend for a higher recurrence rate in children younger than 15 years compared with older patients. Recurrence rates were also reported to be higher in children by several authors especially in younger children. 13,18 Gibbs et al 13 reported a higher recurrence rate in children with ABCs 10 years or younger versus patients ranging in age from 11 to 58 years. In addition, Freiberg et al 18 reported recurrences in 5 of 7 children (e10 years) after surgery. On the contrary, Dormans et al 19 stated that the difference in persistence or recurrence rates based on age comparing the younger and older ages in pediatric patient group was not statistically significant in their series of 45 patients. The purpose of the current study was to summarize our experience in the management of ABC in a large, single-institution series of 56 patients and to determine the possible variables including type of treatment, age of the patient, lesion size, and Capanna classification of the 938 J Pediatr Orthop & Volume 27, Number 8, December 2007
2 J Pediatr Orthop & Volume 27, Number 8, December 2007 lesion which may affect recurrence rates for primary ABCs in children. METHODS In this retrospective study, 71 children were treated for ABC at a single-institution orthopaedic oncology department. The medical records and radiographs of children (e16 years) between March 1986 and November 2006 were reviewed. Sixty-three patients had primary and 8 children had secondary ABCs, with coexistent unicameral bone cyst in 6 cases, nonossifying fibroma in 1 case, and chondroblastoma in 1 case. A total of 15 children were eliminated: 3 because they were lost to follow-up, 1 child because he did not have full data, 8 because they had other bone lesions (secondary), and 3 because they did not have a minimum of 2 years follow-up. This left 56 children with full data for our complete evaluation. Demographic data (sex, age at presentation), clinical data (presenting symptom, location within the bone [Capanna]), surgical records, surgical complications, and radiological data (relationship with the epiphysis, size of the lesion) were reviewed. Measurement of the size (the greatest diameter in cm) was based on computed tomography (CT) scans and magnetic resonance imaging (MRI) scans whenever possible. Capanna and Enneking classifications were used for radiological evaluation of the lesion. The diagnosis of ABC was established with pathological examination in all cases. This series included only patients with primary ABC. Intralesional surgery, mainly curettage through a large cortical window, was the preferred mode of treatment in the vast majority of the patients. Adjuvant treatment modalities used were mainly cauterization and polymethylmethacrylate (PMMA) application. Reconstruction of the cavity was achieved with autogenous, allogenous bone FIGURE 1. A, A 5-year-old boy presented with mild trauma, with pain in the right ankle. Direct lateral radiograph shows an ABC and a fracture of the tibia. B, Four months after treatment with curettage and bone grafting. C, One year later, plain radiograph revealing recurrence of the ABC. D, An axial-view CT of the recurrent lesion. E, One year after repeat curettage and bone grafting. F, Lateral radiograph obtained at the 4-year follow-up shows a well-healing and remodeled tibia. * 2007 Lippincott Williams & Wilkins 939
3 BazarNr etal J Pediatr Orthop & Volume 27, Number 8, December 2007 grafts, and occasionally with bone cement. En bloc excision of the bone was used in expandable bones such as fibula or in cases with gross destruction of the bone with no possibility of intralesional procedures. Preoperative embolization was used in 4 patients for decreasing the amount of intraoperative hemorrhage. Phenol or hydrogen peroxide was not used as adjuvant treatment modalities. All of the operations were performed by 2 senior surgeons. Data were analyzed initially with Student t test and Pearson W 2 test using SPSS for Windows release 11.5 (SPSS Inc, Chicago, IL). A logistic regression analysis model was used for multivariate analysis. Statistical significance was defined as P G Risk factors with a P G 0.05 were assumed to be independent risk factors associated with the event of recurrence. Odds ratios were also determined. The following variables were analyzed: patient age at time of diagnosis, juxtaphyseal location, the lesion size, and previous surgery. Age was categorized as follows: 5 years or younger = 1, 5 to 10 years = 2, older than 10 years = 3, and radiological Capanna classification was classified as follows: central type 2 = 1, other types (1, 3, 4, or 5) = 2. The lesion was accepted as juxtaphyseal when there was direct contact with the physis on radiological examination. Fisher exact test was done to determine the statistical significance of the difference in recurrence rates between the groups. RESULTS There were 33 male patients at a mean age of 10.5 years (range, 3Y16 years) and 23 female patients at a mean age of 10.8 years (range, 1.5Y16 years). Nine patients were younger than 5 years, 17 were between 5 and 10 years, and 30 were older than 10 years. The main presenting symptom was pain in 28 patients followed by swelling (9 cases) and tender mass (9 cases). Aneurysmal bone cysts were found incidentally in 3 patients, and a pathological fracture was the first sign in 7 cases (Fig. 1A). The duration of symptoms varied from 1 to 12 months, with a mean duration of 3.2 months. The humerus (10 cases), tibia (9 cases), femur (8 cases), fibula (8 cases), radius (3 cases), pelvis (5 cases), clavicle (2 cases), ulna (2 cases), and small bones of hand and feet (4 cases) were the most common locations. The sacrum and C7 were the locations of 1 cyst. FIGURE 2. A, An ABC located in proximal humerus underwent curettage and bone grafting. Direct radiograph in the early postoperative period (6 weeks) revealing the grafts and expanded cortex. B, Nine months postoperatively, expansion of the lesion indicating recurrence. C, Six months after repeat curettage and grafting. D, Anteroposterior radiograph obtained at the 6-year follow-up shows a remodeled humerus. 940 * 2007 Lippincott Williams & Wilkins
4 J Pediatr Orthop & Volume 27, Number 8, December 2007 TABLE 1. Percentage of Recurrence Based on Age, Epiphyseal Involvement, Radiological Stage, Previous Operation, and Type of Operation Patients, n Recurrence, n Percent, % Age, y e Epiphyseal involvement Absent Present Capanna stage Enneking stage Previous operation Absent Present Type of management 1 (Intralesional) (Excision) (Radiation therapy) (Intralesional with adjuvant) According to Capanna classification, 9 cysts were type 1, 33 were type 2, 11 were type 3, 1 was type 4, and 2 were type 5. Aneurysmal bone cyst as a benign bone lesion was classified according to Enneking staging system as inactive, active, and aggressive lesions. The lesions were inactive in 12 cases, active in 31 cases, and aggressive in 13 cases. Thirtyseven lesions (66.1%) were in contact with the growth plate. The mean size of the lesion was 5.52 cm (range, 2Y12 cm) in the whole group and similar in both recurrent (5.44 cm) and nonrecurrent cases (5.53 cm). Six radionuclide technetium bone scans were performed, and a hypersignal was observed in all lesions. Magnetic resonance imaging examination was performed in 35 patients, in which typical showed fluid-fluid levels in 25 of them. Ten patients had previous surgery, mainly open biopsy or incomplete intralesional procedures. The most common initial treatment was curettage associated with bone grafting performed in 23 patients (41.1%) (Fig. 1B). En bloc resection was performed in 19 patients (33.9%). Radiation therapy was used in 2 cases with sacral and proximal humeral involvement. The case with proximal humeral involvement had 2 previous surgeries: one open biopsy and one contaminated intralesional curettage. Cauterization and or PMMA application were used as adjuvants in 12 patients. Nine of the 56 children had recurrences, defined as a persistent radiolucent lesion that either progressed radiographically (recurrence) or ultimately involved more than one-third of the originally involved bone (persistence). The persistent and recurrent lesions were located in the proximal humerus (6 patients), in the tibia (2 patients), and in the femur (1 patient) (Figs. 1C and 2A, B). The average time span between surgery and the initial recurrence was 15 months (range, 6Y50 months). Seven lesions recurred once, and 2 lesions recurred twice. These recurrences occurred in 6 cases after simple curettage, in 2 cases after curettage together with adjuvant therapy, and in 1 case with radiation therapy (Fig. 1D). Of the 9 recurrences, 1 case was Capanna type 1, 7 type 2, and 1 type 3. According to the Enneking classification, one had inactive, 7 patients had active, and 1 patient had aggressive lesion. Seven of 9 recurrences had epiphyseal contact. Of the 9 patients, 5 were 5 years old or younger, 2 were between 5 and 10 years, and 2 were older than 10 years. Four lesions recurred out of 7 pathological fractures (Table 1). Recurrent lesions were treated with repeat curettage and bone grafting (6 patients) and with adjuvant cauterization or PMMA in 3 patients (Fig. 1E). Only 2 of the 6 patients had additional recurrence: one underwent excision of lesion and structural grafting (proximal humeral lesion) and the other had curettage with adjuvant cauterization. Both had no further recurrences after more than 6 years followup. There were 8 complications, including 4 deformities, 2 limb inequalities, 1 superficial infection which recovered with parenteral antibiotics, and 1 transient peroneal nerve paralysis after resection of proximal fibula which recovered within 4 months. In 2 cases, residual appearances were observed in direct roentgenograms which were closely followed up for more than 2 years with CT and MRI revealing the recovered lesion without further progression of the lesion. At the longest follow-up, all resumed normal daily activities (Figs. 1F and 2C, D). The patients had a mean follow-up of 48.1 months (range, 24Y194 months) from the date of the initial surgery. Data were analyzed to study the recurrence rate as a function of age, size of the lesion, juxtaphyseal location, and Capanna classification with categorization. The size of the lesion (Mann-Whitney U test, P = 0.973) and juxtaphyseal location were found to be insignificant (Fisher exact test, P = 0.703). When Capanna classification was considered, there were no significant increases in the central type when compared with others (P = 0.282). Recurrence occurred in 5 of 9 children who were 5 years old or younger. When logistic regression analysis model was used for multivariate analysis, the difference in the persistence or recurrence rates in the younger age group (5 years) was statistically significant (P = 0.021) (Table 2). However, the recurrence rate in the age group between 5 and 10 years was not TABLE 2. Multiple Logistic Regression Model of Risk Factors for Recurrence Risk Factor P Odds Ratio 95% Confidence Interval Previous surgery Y43.21 Age e5 y Y94.20 * 2007 Lippincott Williams & Wilkins 941
5 BazarNr etal J Pediatr Orthop & Volume 27, Number 8, December 2007 statistically significant (P = 0.694). Previous surgery also increases the recurrence rates (Fisher exact test, P = 0.006). DISCUSSION Aneurysmal bone cyst is an uncommon primary nonneoplastic but locally destructive lesion of the bone with a prevalence of 1.4 cases per 100,000 individuals. 1,2,4,15 However, the real incidence of ABCs may be underestimated due to spontaneous healing and clinically silent lesions which may be detected only incidentally. 1,3 Although ABC may occur in virtually any bone at any age, more than half of the ABCs present in the long bones, and about 80% of the cases are seen before the age of 20 years. 16,20Y22 Cottalorda et al 3 found no main differences in site distribution among children and the adult population. In our series, tubular bones were more commonly affected as in other series. 2,19 Otherwise, the humerus was slightly more involved instead of more usual localizations such as in the femur and tibia. Aneurysmal bone cyst usually has a slight female predominance; however, vice versa was reported in patients before the age of 14 years. 1,3 There was a male predominance with a male/female ratio of 3:2 in our series. Among pediatric patients, the lesion is reported to be rare in patients younger than 5 years. 2 The lesion rate before the age of 5 years was 16.1% in our series which was comparable to previous pediatric series. 2,3,19 Most of the patients presented with pain and swelling as the typical clinical features; in addition, pathological fracture was seen in 12.5% of our patients. 2Y4 Radiographic features of ABC are not characteristic and show remarkable similarities with other benign cystic lesions, and it also may be secondary to various benign and malignant conditions. In these situations, the presence of septations and multiple fluid-to-fluid levels seen in MRI scans is reliable in achieving the diagnosis as observed in 71% of the MRI scans obtained. 23 Thirteen (61%) of 21 patients were in contact with the growth plate in the multicenter study of Cottalorda et al, 3 similar to our study (66%). Besides age, pathological behavior of the lesion and radiological characteristics may have prognostic implications on recurrence. The Capanna subdivision into morphological types is an important prognostic factor in previous series. The central forms have a higher recurrence rate than the peripheral forms. 3 All the recurrences in their series were in active or aggressive tumors. There was only 1 recurrence in the inactive lesions. Although most of the recurrent lesions were active and had central form of Capanna morphological types, there were no statistically significant differences found after categorization (P = 0.282). Treatment modalities for this benign condition vary from minimally invasive procedures such as the percutaneous injection of steroid, calcitonin, or fibrosing agentvalcoholic zeinvto en bloc resection in an expandable bone such as the fibula, clavicle, or rib. 5,11,24,25,26 There were no recurrences observed in resected lesions (19 cases); however, most tumors are not located in expandable bones, and therefore, less radical surgery was used for management of these lesions. Intralesional curettage is a suitable alternative which is the most commonly used treatment modality as in our series (41%), and cure was achieved with 1 surgery in 17 of 23 patients. 27 The quality of the curettage is almost impossible 942 to standardize because some of the lesions are in contact with the growth plate which highlights surgeon-related factors and single-institution series. Previous surgery such as open biopsy or inadequate intralesional excision was found to be significant factors in recurrence. Patients with previous surgery were 7 times more likely to have a recurrence. It may lead to increased recurrence rates by possible contamination or by fibrosis causing difficulty in distinction of healthy and diseased tissues. The recurrence rates of surgical treatment vary and range from 10% to 59%. 5,11,13,17,18 Adjuvants such as cauterization and PMMA application were used to increase the efficacy of curettage. 22,28 In adjuvant group, recurrence was slightly lower but still close to simple curettage and bone grafting (22% and 26%, respectively). Several authors reported that tumor recurrence was more frequent in the younger patients. 4,22,29 Biesecker et al 17 reported a trend between young age (G15 years) and higher recurrence in their series of 66 cases, and Vergel De Dios 16 stated that more than 90% of recurrent lesions occurred in patients younger than 20 years of age in more than 200 cases. In the subgroup of pediatric patients, recurrence rates after intralesional procedures may rise up to 50% to 71% in children younger than 10 years and 75% in children younger than 5 years. 2,13,18 Zehetgruber et al 30 evaluated 73 cases of ABCs in their epidemiological study and stated age and sex were associated with higher risk of recurrence. Similarly, age was found to be a prognostic factor for recurrence in our series. Despite that there was a slight male predominance with a male/female ratio of 5:4 in the recurrent group, the difference was not significant. Most of the recurrences were active and aggressive lesions and occurred at the juxtaepiphyseal or meta-epiphyseal region. 1,13,18 We found a 55% recurrence rate in the youngest age group (G5 years) which was comparable with previous series. Two possible explanations suggested first are that the clinical and pathological behavior of ABCs in younger patients is more aggressive and, second, that the higher recurrence rate may be due to excessive caution on the part of the surgeon when faced with a potential growth arrest in such a very young patient. 2 Therefore, the number and the experience of the surgeons may vary among multicenter series and make the results difficult to compare. The study has its own limitations; although 2 surgeons performed all operations of this large series, close relationship of the lesions with the epiphysis makes the curettage difficult to standardize among patients. However, this would not limit the validity of the data, as the center- and surgeon-related factors were minimized in a single-center study. There are several reports which did not support these findings. Dormans et al 19 did not find any statistically significant difference between the younger (G10 years) and older age groups (G10 years) for primary ABC persistence or recurrence in their study of 45 ABCs. Similarly, Cottalorda et al 3 reported that ABCs in children 5 years or younger did not seem more aggressive than in older children and concluded that more aggressive operative intervention does not appear to be indicated due to acceptable recurrence rates. In our study, we looked at primary ABCs in a large population * 2007 Lippincott Williams & Wilkins
6 J Pediatr Orthop & Volume 27, Number 8, December 2007 of the pediatric age group treated consecutively by 2 senior surgeons. Persistence or recurrence (the need for additional surgery) occurred in 5 of 9 children who were 5 years or younger and in 2 patients each in the age groups of 5 to 10 years and those older than 10 years together including 47 patients. There was a statistically significant difference between the youngest age group and other groups concerning primary ABC persistence or recurrence. As a conclusion, the current study shows an 82% cure rate after the initial surgery which was comparable but slightly lower than the mean recurrence rate in the literature review. The clinical behavior of ABCs in younger patients seemed to be more aggressive than in older children. Although statistically insignificant, recurrence is more common in juxtaphyseal location where the cyst removal is difficult, and orthopaedic surgeons dealing with such lesions should be familiar in working near open growth plates. Young age (e5 years) is a risk factor for persistence or recurrence, and the patients family should be warned about this possibility. We think that patients with various risk factors including age or admission with a previous surgery should be treated first with intralesional curettage. Recurrence rates are generally acceptable and may be cured with intralesional procedures. REFERENCES 1. Leithner A, Windhager R, Lang S, et al. Aneurysmal bone cyst. A population based epidemiologic study and literature review. Clin Orthop Relat Res. 1999;363:176Y Ramirez AR, Stanton RP. Aneurysmal Bone Cyst in 29 Children. J Pediatr Orthop. 2002;22:533Y Cottalorda J, Kohler R, Gauzy JS, et al. 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