Rhabdomyosarcoma in Children and Adolescents: Patterns and Risk Factors of Distant Metastasis
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1 Pediatric Imaging Original Research Kim et al. Distant Metastasis of Rhabdomyosarcoma in Children and Adolescents Pediatric Imaging Original Research Jeong Rye Kim 1 Hee Mang Yoon 1 Kyung-Nam Koh 2 Ah Young Jung 1 Young Ah Cho 1 Jin Seong Lee 1 Kim JR, Yoon HM, Koh KN, Jung AY, Cho YA, Lee JS Keywords: children, distant metastasis, prognosis, rhabdomyosarcoma, risk factor DOI: /AJR Received October 1, 2016; accepted after revision January 22, Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, 88 Olympic-ro 43-gil, Songpa-gu, Seoul 05505, Korea. Address correspondence to H. M. Yoon (espoirhm@gmail.com). 2 Division of Pediatric Hematology/Oncology, Department of Pediatrics, Asan Medical Center Children s Hospital, University of Ulsan College of Medicine, Seoul, Korea. Supplemental Data Available online at AJR 2017; 209: X/17/ American Roentgen Ray Society Rhabdomyosarcoma in Children and Adolescents: Patterns and Risk Factors of Distant Metastasis OBJECTIVE. The objective of this study is to evaluate patterns of distant metastasis and identified factors that may increase the risk of distant metastasis in pediatric patients with rhabdomyosarcoma. MATERIALS AND METHODS. This retrospective study included 69 patients (age, 20 years) who had rhabdomyosarcoma diagnosed between January 2000 and February Various imaging features, including distant metastasis, were evaluated on initial and follow-up imaging studies. Differences in the distribution of distant metastasis on the basis of the primary location were analyzed. Logistic regression analysis was performed to identify factors associated with distant metastasis. RESULTS. Twenty-six of the 69 patients (37.7%) had distant metastasis. Nineteen of the 26 patients had distant metastasis noted at initial presentation, and 15 of the 26 patients had new metastasis noted during follow-up. The most common site of metastasis was bone (n = 14), followed by lung (n = 12) and distant lymph nodes (n = 9). Lymph node metastasis more frequently developed in patients with primary rhabdomyosarcoma in an extremity than in patients with primary rhabdomyosarcoma that developed at other sites (p = 0.003). Of 15 patients who had metastasis during follow-up, nine (60%) did not appear to have simultaneous locoregional recurrence at the time of the discovery of distant metastasis. Older age at presentation and unfavorable sites of the primary tumor were significantly associated with distant metastasis in multivariate analysis. CONCLUSION. Distant metastasis of rhabdomyosarcomas in pediatric patients showed different patterns according to the location of the primary tumor and even occurred without local recurrence. R habdomyosarcoma is the most commonly occurring soft-tissue sarcoma in children, representing 3 4% of all cancers that develop during childhood [1]. Important prognostic factors for rhabdomyosarcoma include not only characteristics of the primary tumor, such as its location, size, and resectability, but also the occurrence of regional relapse or distant metastasis [2 7]. The rate of distant metastasis ranges from 14% to 28% [8, 9]. The reported survival rate of patients with category I and group 1 rhabdomyosarcoma was lower for patients with distant metastasis (30%) than for those with local (72%) or regional (50%) recurrence [2]. Although debates have existed regarding the benefits of routine imaging surveillance for detecting tumor recurrence in pediatric patients with rhabdomyosarcoma [8, 10 13], it is generally accepted that earlier detection of distant metastasis and appropriate treatment may offer a potential opportunity to improve patient survival. Therefore, imaging surveillance of patients with rhabdomyosarcoma at the time of presentation as well as during follow-up is essential for assigning risk-based stratification and detecting local recurrence or distant metastasis or both. However, limitations exist regarding intensive imaging surveillance of pediatric patients because of their repeated exposure to ionizing radiation and anesthetic agents administered for sedation, especially among younger children, and because of the high cost [14]. Considering these obstacles, an appropriate strategy for imaging surveillance of pediatric patients with rhabdomyosarcoma is required, and this imaging strategy should be based on the characteristics of distant metastasis. A previous study reported the initial factors that allow prediction of the pattern and AJR:209, August
2 Kim et al. Between January 2000 and February 2016 Diagnostic code: rhabdomyosarcoma Demographic code for age 20 years 80 Patients 69 Patients Exclusion (n = 11) 1. Final diagnosis as other pathology (n = 4) 2. Initial imaging studies of the primary tumor were not available (n = 7) risk of relapse in patients with localized rhabdomyosarcoma [8]. However, that study primarily focused on local recurrence in patients with localized rhabdomyosarcoma. To our knowledge, only a limited number of studies exist that evaluate the pattern of distant metastasis in pediatric patients with rhabdomyosarcoma. Therefore, the purpose of the present study is to assess the pattern of distant metastasis and identify factors that may increase the risk of distant metastasis in pediatric patients with rhabdomyosarcoma. Materials and Methods Patients The institutional review board at Asan Medical Center approved this retrospective study and waived the requirement for informed consent. We performed a systematic computerized search of the database at our tertiary referral hospital from January 2000 to February 2016, to identify patients with rhabdomyosarcoma who were 20 years old or younger. We identified 80 consecutive patients and then selected patients for inclusion in the study on the basis of the following criteria: the patient had rhabdomyosarcoma diagnosed on the basis of histopathologic findings, initial diagnosis was made when the patient was 20 years old or younger, and imaging studies used in the diagnosis of primary rhabdomyosarcoma were available. We excluded 11 of the 80 patients because four of the patients had a final diagnosis of Ewing sarcoma or primitive neuroectodermal tumor and because seven of the patients were referred to our hospital after receiving treatment but did not have initial imaging studies of the primary tumor available (Fig. 1). Fig. 1 Flowchart of patient selection for study. Tumor Classification Tumors were classified in accordance with the pretreatment TNM system (Table S1, a supplemental table, can be viewed in the AJR electronic supplement to this article, available at www. ajronline.org) [3] and the surgical and pathologic clinical grouping system established by the Intergroup Rhabdomyosarcoma Study (IRS) (Table S2, a supplemental table, can be viewed in the AJR electronic supplement to this article, available at [5, 15]. The locations of the primary tumors were categorized as favorable and unfavorable sites, on the basis of the IRS-modified pretreatment TNM system [3, 5]. Favorable sites include the orbit, head and neck (excluding parameningeal sites), genitourinary system (excluding the bladder and prostate), and biliary tract. Unfavorable sites include the bladder and prostate, extremities, cranial parameningeal sites, and other sites, including the trunk and retroperitoneum [5]. Fig. 2 Kaplan-Meier curve of overall survival for patients with localized disease (black line) and patients with distant metastases (gray line). Median survival was 57 months for patients with localized disease and 26.5 months for patients with distant metastasis (p = 0.002). Overall Survival (%) Image Acquisition and Analysis During the 16-year study, various CT, MRI, and PET/CT scanners were used at our hospital as well as at multiple other hospitals that referred patients to our hospital. All available images, including CT (n = 67), MR (n = 38), and PET/CT images (n = 26), obtained at the time of the initial diagnosis were retrospectively reviewed in consensus by two pediatric radiologists. At the time of the initial diagnosis, we evaluated the images with regard to tumor size (i.e., the largest dimension of the tumor), location, pattern of enhancement (homogeneous vs heterogeneous), margin (well defined vs poorly defined), presence of local invasion in the adjacent organs, and presence of necrosis in the primary tumors. According to a previous study [16], tumors with uniform enhancement pattern in more than 90% of the tumor area, as determined by visual inspection, were categorized as having a homogeneous enhancement pattern, whereas all other tumors were classified as having a heterogeneous enhancement pattern. If a smooth margin without spiculation or infiltration into more than 75% of the tumor perimeter was observed, the tumor was categorized as having a well-defined margin. If the tumor did not meet these criteria, it was categorized as having a poorly defined margin. If an unenhanced portion existed in the center of the tumor, we considered this finding to indicate the presence of necrosis. When tumors directly infiltrated the adjacent organs, causing obliteration of the fat plane between the primary tumor and the adjacent organ, it was regarded as local invasion. The presence of regional lymph node (LN) metastasis and distant metastasis was also evaluated at initial diagnosis. LN metastasis was defined using the following criteria: histologic confirmation, a short diameter of more than 1.5 cm, the presence of a necrotic portion, and avid FDG uptake on PET/CT [16, 17]. LN metastasis other than regional LN metastasis was defined as distant metastasis. The changes in primary tumors, including Time (mo) 410 AJR:209, August 2017
3 tumor size, were evaluated during follow-up. Locoregional recurrence was defined as recurrence Data for quantitative variables were present- Characteristics of Patients Statistical Analysis TABLE 1: Demographic and Clinical Distant Metastasis of Rhabdomyosarcoma in Children and Adolescents that was located either at or adjacent to the primary ed as the mean (± SD) value or the median value at Baseline tumor site and that included regional LNs and the range. Kaplan-Meier curves were used to Demographic or [6, 8]. The location and number of involved distant evaluate the cumulative survival curves and were Clinical Characteristic Value metastasis sites were evaluated at the time of compared using the log-rank test. Differences in the initial diagnosis and during follow-up. Distant the distribution of distant metastasis according to Age (y) metastasis was diagnosed by pathologic confirmation or by comparison of follow-up imaging studies with clinical medical records. Patients who had the location of the primary tumor were analyzed using the Fisher exact test, followed by the multiple comparison procedure with an adjusted p value Mean ± SD Range Sex 8.0 ± (p < was considered to denote statistical metastatic disease develop either during or soon after completion of therapy were considered to significance). Univariate and multivariate analyses Male 40 have metastatic disease. First metastasis was defined as metastasis occurring in a patient who had localized rhabdomyosarcoma for identifying factors associated with distant metastasis were performed using logistic regression analysis. The risk was expressed as an odds ratio Female Tumor size (cm) Mean ± SD ± 3.5 seen on the initial presentation and (OR) with a 95% CI. Multivariate analysis was per- for whom first detection of distant metastasis occurred formed using variables that showed statistical significance Range during follow-up. Second metastasis was defined as another new metastatic event occurring after first metastasis developed or as metastatic in the univariate analysis by use of the backward elimination manner. Statistical differences were considered statistically significant at < 5 5 Tumor histologic subtype 28 (40.6) 41 (59.4) noted during follow-up [18]. rhabdomyosarcoma noted on initial presentation p < Statistical software (SPSS software, version 20.0, SPSS-IBM) was used for the analyses. of a patient who had additional distant metastasis Embryonal Alveolar 49 (71.0) 20 (29.0) Treatment Of the 69 patients in our study, 18 were treated in accordance with the Intergroup Rhabdomyosarcoma Study IV (IRS-IV) protocol [19, 20] until July 2005, and the other 51 patients were treated in accordance with the Intergroup Rhabdomyosarcoma Study V (IRS-V) protocol, depending on the risk stratification [7, 19, 21]. A total of 39 of the 69 patients underwent radiotherapy for local control, palliative therapy, or both. Most of the patients underwent surgery (n = 61). Thirteen of the 69 patients underwent various treatments or combinations of treatments, including an ICE (ifosfamide, carboplatin, and etoposide) protocol (n = 11), treatment with cyclophosphamide and topotecan (n = 5), peripheral blood stem cell transplantation (n = 2), treatment with docetaxel and gemcitabine (n = 1), and treatment with cetuximab (n = 1), as a result of refractory rhabdomyosarcoma that occurred in spite of chemotherapy, in accordance with IRS-IV or IRS-V. Time to Detection of Metastasis and Patient Survival The time to metastasis during follow-up was evaluated. The median time to first metastasis was defined as the interval between the date of acquisition of the initial image of the primary tumor and the time of the appearance of the first metastatic event seen on follow-up imaging studies. The median time to the second distant metastasis was defined as the interval between the date of the first metastatic event and the date of the second metastatic event. For evaluation of overall survival, the interval between the primary diagnosis and either death of the patient for any reason or the last follow-up was calculated. Results Characteristics of the Patients and the Primary Tumors A total 69 patients (40 male patients and 29 female patients; mean age, 8.0 ± 6.1 years) were included in our study. Descriptive characteristics of the patients are presented in Table 1. There were 49 embryonal subtypes and 20 alveolar subtypes of rhabdomyosarcoma. The primary tumors originated from the trunk in 35 patients (50.7%), the head and neck in 24 patients (34.8%), and an extremity in 10 patients (14.5%). The specific locations of the primary tumors are presented in Table S3 (a supplemental table, which can be viewed in the AJR electronic supplement to this article, available at Fiftythree patients (76.8%) had primary tumors in unfavorable sites, and 16 patients (23.2%) had them in favorable sites. Most tumors had a poorly defined margin (81.2%) and heterogeneous enhancement (91.3%). Necrosis and local invasion were observed in 32 patients (46.4%) and 45 patients (65.2%), respectively. According to the IRS-modified pretreatment TNM system, 16 patients (23.2%) had rhabdomyosarcoma classified as category I, 10 (14.5%) had category II, 24 (34.8%) had category III, and 19 (27.5%) had category IV. In terms of the IRS clinical group classification, 12 (17.4%), 12 (17.4%), 26 (37.7%), and 19 (27.5%) patients had rhabdomyosarcoma classified as belonging to groups I, II, III, and IV, respectively. Location of primary tumor Head and neck 24 (34.8) Trunk 35 (50.7) Extremity 10 (14.5) Location a Favorable 16 (23.2) Unfavorable 52 (75.4) Tumor margin Well defined 13 (18.8) Poorly defined 56 (81.2) Tumor enhancement Homogeneous 6 (8.7) Heterogeneous 63 (91.3) Tumor necrosis Present 32 (46.4) Absent 37 (53.6) Local invasion Present 45 (65.2) Absent 24 (34.8) Regional lymph node metastasis Present 19 (27.5) Absent 50 (72.5) Note Except where otherwise indicated, data are the number (%) of patients. a Classified according to the Intergroup Rhabdomyosarcoma Study modified TNM categorization system. Patient Survival During the mean follow-up of 59.3 months, eight patients died and 30 patients remained alive. The other 31 patients were lost to follow-up. The median overall survival was 42.0 months (range, months). The median survival of patients with localized disease (n = 43; 57 months) was statistically significantly AJR:209, August
4 Kim et al. TABLE 2: Locations of Metastasis in Patients With Rhabdomyosarcoma Finding Histologic subtype All Patients With Metastasis a (26/69; 37.7%) Patients With Metastasis at Initial Presentation (19/69; 27.5%) Patients With First Metastasis b (7/50; 14.0%) Patients With Second Metastasis c (9/26; 34.6%) Embryonal Alveolar Location of metastasis Bone Lung Distant lymph node Peritoneum Breast Pleura CNS Skin Pancreas Retroperitoneum Soft tissue 1 d 1 d 0 1 e Testis Liver Salivary gland Perineum Epidural space of spinal canal Note Data are the number of patients. a The mean follow-up for the evaluation of overall metastasis was 42.0 months (range, months). b First metastasis was defined as metastasis occurring in a patient who had localized rhabdomyosarcoma seen on the initial presentation and for whom first detection of distant metastasis occurred during follow-up. The mean follow-up for the evaluation of first metastasis was 54.5 months (range, months). c Second metastasis was defined as another new metastatic event occurring after first metastasis or as metastatic rhabdomyosarcoma noted on initial presentation of a patient who had additional distant metastasis noted during follow-up. The mean follow-up for the evaluation of second metastasis was 16.5 months (range, months). d Posterior neck and psoas muscles. e Posterior neck muscle. TABLE 3: Locations of All Cases of Distant Metastases in 26 of 69 Patients With Rhabdomyosarcoma, According to Primary Tumor Site Location Head and Neck (8/24; 33.3%) Trunk (13/35; 37.1%) Extremity (5/10; 50.0%) p a Bone 5 (62.5) 8 (61.5) 1 (20.0) Lung 5 (62.5) 4 (7.7) 3 (60.0) Distant lymph node b 1 (12.5) 3 (23.1) 5 (100) Peritoneum 0 (0) 4 (30.8) 1 (20.0) Breast 2 (25.0) 0 (0) 0 (0) Pleura 1 (12.5) 2 (15.4) 1 (20.0) CNS 0 (0) 2 (15.4) 1 (20.0) Skin 0 (0) 2 (15.4) 0 (0) Other 1 (12.5) c 5 (38.7) d 3 (60.0) e Note Except where indicated otherwise, data are number (%) of patients. The primary tumors originated from the trunk in 35 patients (50.7%), the head and neck in 24 patients (34.8%), and an extremity in 10 patients (14.5%). a Fisher exact test for comparison of the three primary sites. b Distant lymph node metastasis was more frequently observed in an extremity than in other sites (for head and neck vs trunk, p = 0.572; for trunk vs extremity, p = 0.011; and for head and neck vs extremity, p = 0.004). c One in salivary gland. d One each in retroperitoneum, liver, testis, perineum, and pancreas. e One each in soft tissue (i.e., posterior neck and psoas muscles), epidural space of the spinal canal, and pancreas. 412 AJR:209, August 2017
5 Distant Metastasis of Rhabdomyosarcoma in Children and Adolescents longer than that of patients with distant metastasis (n = 26; 26.5 months) (p = 0.002) (Fig. 2). Overall Metastasis of Rhabdomyosarcoma A total of 26 of the 69 patients (37.7%) had metastatic disease at initial presentation (n = 19) or detected during a follow-up period (n = 16) (Table 2). Distant metastasis was found in 14 patients with the embryonal subtype and 12 patients with the alveolar subtype. The most common site of metastasis was bone (n = 14), followed by lung (n = 12), and distant LN (n = 9). Table 3 shows the detailed locations of distant metastasis according to the primary tumor site. LN metastasis more frequently developed in patients with rhabdomyosarcomas originating in the extremities rather than in the head and neck (adjusted p = 0.004) and trunk (adjusted p = 0.011). There were two adolescent female patients who had distant metastasis in their breasts, and the histologic subtype of their primary tumors was the alveolar subtype. Distant Metastasis at the Initial Presentation Nineteen of the 69 patients (27.5%) had metastatic disease at initial presentation (Table 2). All of the patients had primary tumors in unfavorable locations. Ten patients had distant metastasis in only one location, four patients in two different locations, three patients in three different locations, one patient in four locations, and one patient in five different locations. The most common site of metastasis was bone (n = 10), followed by a distant LN (n = 8). First Distant Metastatic Event Detected During Follow-Up Fifty patients who had only local disease at their initial presentation were monitored for evaluation of the first distant metastatic event. The median follow-up was 54.5 months (range, months). The median time to metastasis was 14.0 months (1 85 months) (Fig. 3). Seven of 50 patients (14.0%) with local disease detected at initial presentation had distant metastasis develop during follow-up (Table 2). Five patients had primary tumors in unfavorable locations, and two patients had them in favorable locations. The most common location of metastasis was the pleura (n = 3), followed by lung and bone (n = 2, respectively). Five patients had distant metastasis in one location, and two patients had them in three different locations. Second Distant Metastatic Event Detected During Follow-Up The median follow-up for the detection of second metastasis in 26 patients who had distant metastasis at their initial presentation (n = 19) or during follow-up (n = 7) was 16.5 months (range, months). The median interval between the detection of first metastasis and the detection of the second distant metastasis was 9.0 months (1 30 months) (Fig. 3). Nine of the 26 patients (34.6%) with distant metastatic rhabdomyosarcoma developed the second distant metastasis during follow-up (Table 2). All nine patients had primary tumors in unfavorable locations. The most common location of second metastasis was a distant LN (n = 3), followed by bone, lung, and brain (n = 2, respectively). Seven patients had the second metastatic event develop in one location and two patients had it occur in two different locations. Status of the Primary Tumor at the Time of Detection of Distant Metastasis Of the 50 patients with localized disease at the time of initial presentation, seven had distant metastasis discovered during follow-up. Of the 19 patients with metastatic disease at initial presentation, eight had additional distant metastasis discovered during follow-up. Overall, 15 patients had distant metastasis discovered during follow-up (mean follow-up, 6 months; range, months). Of these 15 patients, only six (40.0%) had simultaneous, locoregional recurrence at the time of detection of the distant metastasis. Two of the 15 patients (13.3%) had a stable primary tumors, and two other patients (13.3%) had a decrease in the size of their primary tumors. The other five patients (33.3%) had no remnant or recurrent tumor at the primary tumor site (Fig. 4). Factors Associated With Distant Metastasis Table 4 shows the results of univariate and multivariate analyses for identifying the factors associated with distant metastasis. Four factors, including patient age at initial presentation, alveolar histopathologic subtype, unfavorable sites of the primary tumor, and the presence of regional LN metastasis at the initial presentation, had statistical significance on univariate analysis. According to multivariate analysis, independent predictive factors associated with distant metastasis were older patient age at presentation (OR, 1.172; p = 0.002) and unfavorable sites of the primary tumor (OR, 8.190; p = 0.016). Discussion The present study showed that a total of 37.7% of the patients had distant metasta- TABLE 4: Findings From Univariate and Multivariate Analyses Performed to Identify Factors Associated With Distant Metastasis Univariate Analysis Multivariate Analysis Factor at Initial Presentation Odds Ratio (95% CI) p Odds Ratio (95% CI) p Patient age ( ) ( ) Patient sex ( ) Tumor size ( ) Histopathologic subtype Embryonal Alveolar ( ) ( ) Anatomic location of the primary tumor Head and neck Trunk ( ) Extremity ( ) Location a Favorable Unfavorable ( ) ( ) Tumor margin ( ) Enhancement ( ) Necrosis ( ) Local invasion ( ) Regional lymph node metastasis ( ) ( ) a Classified according to the Intergroup Rhabdomyosarcoma Study modified TNM categorization system. 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6 Kim et al. No. of Patients Time of Metastasis (mo) Fig. 3 Time to first and second metastasis. Bar graph shows that time to first metastasis for seven patients who had local disease only at initial presentation was 1 month for two patients and 7 months, 14 months, 19 months, 29 months, and 85 months for remaining five patients (white bars). Median time to first metastasis was 14 months (range, 1 85 months). For nine patients, time to second metastasis (interval from detection of first metastasis to detection of second metastasis) was 1 month, 6 months, 7 months, 8 months, 9 months, 11 months, 24 months, 29 months, and 30 months (black bars). Median time to second metastasis from detection of first metastasis was 9 months (range, 1 30 months). sis, and most of these patients (27.5%) had metastasis identified at the time of initial diagnosis. The most common site of metastasis was bone, followed by lung and LN. Patients with the primary tumor in an extremity tended to have distant metastasis in the LNs. Ten of 15 patients showed distant metastasis without locoregional recurrence occurring during follow-up. Older patient age at presentation and unfavorable primary tumor sites were the factors associated with the development of distant metastasis. To our knowledge, only a limited number of studies focus on the initial factors associated with distant metastasis in patients with rhabdomyosarcomas. Older patient age at presentation, unfavorable sites of the primary tumor, the size of the primary tumor, an alveolar subtype, and the presence of regional LN metastasis have been recognized as prognostic factors for rhabdomyosarcoma [4, 6, 8, 22, 23]. According to a study by Dantonello et al. [8], older patient age at presentation, alveolar subtype, tumor size, postsurgical category, and omission of radiotherapy were identified as factors associated with an increased risk of relapse. In our study, patient age at presentation and unfavorable sites of the primary tumor were significantly associated with distant metastasis; however, the size of the primary tumor, the alveolar subtype, and the presence of regional LN metastasis were not significant factors associated with distant metastasis. Our results might be explained by the presumption that tumor size, histopathologic subtype, and the presence of regional LN metastasis may be more closely related to other factors, such as locoregional recurrence, treatment response, or the growth rate of the tumor, than to the development of distant metastasis. In this study, 27.5% of the patients had distant metastasis at the time of their initial presentation, a finding that was similar to that seen in previous studies [8, 9, 24]. Regarding distant metastasis detected during followup, a total of 14.0% of patients with localized disease had distant metastasis develop during follow-up, which was similar to the 10 28% of patients reported in previous studies [8, 9]. In one previous study, the thorax was reported to be the most common site of metastasis; the authors suggested that screening for distant metastasis should be focused on imaging of the thorax, and they doubted the value of bone scans because systemic recurrence affecting bone was rare [8]. On the contrary, the present study revealed that the most common site of distant metastasis was bone, followed by lung. This result was similar to the results of a previous study regarding adult rhabdomyosarcoma, which reported that lung (35.5%) and bone (19.4%) were common sites of metastasis [24]. Moreover, five patients in the present study had distant metastasis in unusual locations, such as the skin, testis, epidural space of the spinal canal, or the perineum. These results may show the need for imaging of other sites rather than the thorax, and imaging surveillance should be tailored and personalized according to each individual patient. We found that LN metastasis developed more frequently in patients with primary tumors in an extremity than in those with primary tumors in the trunk or head and neck. This discovery is in contrast to that of a previous study that showed that LN metastasis was least common in adult patients with rhabdomyosarcoma in an extremity [25]. On the basis of our results, we propose that there might be a different pattern of distant metastasis according to the anatomic location of the primary tumor in pediatric patients with rhabdomyosarcoma. In this study, two patients had distant metastasis in their breasts. These patients were female adolescents who had the alveolar subtype and had multiple metastatic diseases in sites other than their breasts, findings that are consistent with those of previous studies [26, 27]. In contrast to a previous study that reported that the primary tumor occurred at various sites in patients with breast metastasis [27], the primary tumors of these two patients in our study were located in the head and neck. Regarding distant metastasis to the CNS, the primary tumors were located in the trunk and extremity in our study. A previous study reported that, in most patients with CNS metastasis, the primary tumor developed in the parameningeal head and neck area and CNS metastasis was not combined with metastasis in other sites [8]. This finding was quite different from that of our study. A previous study reported that because a large proportion of distant metastases were combined with locoregional relapses, tumordirected follow-up should focus on the primary site in localized rhabdomyosarcoma [8]. However, in our study, 10 of 15 patients (60.0%) did not have locoregional recurrence at the time that their distant metastasis was detected. Two of these 10 patients even had a decrease in the size of their primary tumor at the time that distant metastasis was detected. This mixed response of the primary tumor site and systemic distant metastasis may be explained by occult metastases perhaps becoming overt later while the primary tumor might be controlled by local treatment, such as surgery, radiotherapy, or both. In addition, occult viable tumor cells might remain within the primary tumor site even after local treatment, and they might escape from the primary tumor site and metastasize to distant sites. These results may suggest that only tumor-directed follow-up may result in possible distant metastasis being missed at other sites. A guideline for imaging surveillance of rhabdomyosarcoma has not yet been established; however, some treatment protocols include recommendations that relapse surveillance should be focused on the primary site of the tumor and the common sites of metastasis, including the lung, bone marrow, and bones, with the use of chest CT, bone scanning, bone marrow aspiration and biopsy, and, sometimes, PET/CT [8, 28]. In our study, however, some patients had distant metastases develop in organs other than the lung, bone marrow, and bone. Moreover, more than half of the patients did not have regional recurrence at the time that distant metastasis was detected in the present study. 414 AJR:209, August 2017
7 Distant Metastasis of Rhabdomyosarcoma in Children and Adolescents Therefore, in some cases, distant metastases would be missed if we do conduct follow-up according to the previously mentioned surveillance recommendation [8, 28]. Following this line of thought, whole-body imaging may be one of the reasonable options for screening for distant metastasis throughout the whole body. Several imaging modalities exist for whole-body imaging, such as bone scanning or PET/CT. Bone scanning is a modality for the detection of lesions in the bone only; therefore, it is limited in the detection of extraskeletal lesions. PET/CT can be helpful in the detection of distant metastases; however, its disadvantages include the exposure of children to ionizing radiation. Whole-body MRI, which can cover the whole body and shows good soft-tissue characterization without radiation exposure, can be helpful in the imaging surveillance of pediatric patients with rhabdomyosarcomas. So far, limited numbers of studies exist regarding the feasibility of whole-body MRI examination for patients with rhabdomyosarcoma. Further studies regarding the diagnostic performance and the cost-effectiveness of whole-body MRI for patients with rhabdomyosarcoma are needed. For response assessment and relapse surveillance, the Children s Oncology Group (COG) protocol guidelines recommend imaging of the primary tumor and metastatic sites every 3 months during the first year, every 4 months during the second and third years, and every 6 months during the fourth year after therapy. Patients also undergo two to three sets of evaluations during therapy, depending on their risk group [28]. This guideline is also applicable to our patient population. As shown in Figure 3, distant metastases developed in three patients at 1 month of follow-up and in six patients at 6 to 11 months of follow-up. Thereafter, distant metastases were found at 14, 19, 24, 29, 30, and 85 months of follow-up. According to this observation, we cautiously recommend that follow-up imaging be performed at 1 month after initial presentation, every 3 or 4 months during the first year (to detect early distant metastasis), and every 6 months during the second and third years. Although one patient had distant metastasis develop at 85 months of follow-up, imaging follow-up may be focused on the first 3 years. However, in the future, a multicenter observational study or randomized trial should be conducted with a large number of patients to determine specific guidelines for imaging surveillance of patients with rhabdomyosarcoma, especially regarding the frequency of surveillance and the length of long-term follow-up. This study has several limitations. First, it has a retrospective design and includes a small number of patients. However, these limitations are unavoidable because of the rare nature of rhabdomyosarcoma in pediatric patients. Second, a large number of the patients were lost to follow-up. Third, we did not consider the influence of the treatment of each patient. Patients in our study had received treatment according to IRS-IV or IRS-V protocols; however, there were considerable variations in treatment, especially among patients with refractory rhabdomyosarcoma. Those patients were treated with other regimens, such as an ICE (ifosfamide, carboplatin, and etoposide) protocol, or underwent peripheral blood stem cell transplantation. Hence, the effect of treat- A B C Fig year-old boy who presented with pain and palpable mass in scrotum and had distant metastases without local recurrence at primary site. A, Initial ultrasound image shows two ill-defined masses in right paratesticular area. Surgical resection was performed, and embryonal rhabdomyosarcoma was confirmed by histopathologic examination. After surgery, bone scanning and abdominal CT (not shown) revealed negative findings. B, Follow-up abdominopelvic CT image obtained 14 months after surgery shows newly appearing enlarged retroperitoneal lymph node (arrow) and peritoneal nodule on left side of pelvic cavity (arrowhead). C, Whole-body PET/CT scan shows multifocal increased FDG uptake in axial and proximal appendicular skeletal systems as well as in retroperitoneal lymph node and left peritoneal nodule, which suggests distant metastases. No significant hypermetabolism was noted in right orchiectomy site seen on PET/CT scan, except for physiologic FDG uptake by remaining normal left testis in scrotum. AJR:209, August
8 Kim et al. ment on distant metastasis could not be analyzed. Further studies will be required to elucidate this issue. Last, the patients who had metastatic disease develop either during therapy or soon after completion of therapy could be considered to have treatment failure, not as having new distant metastasis. However, the distinction between failed response to therapy and the development of new metastatic disease was ambiguous in some patients in our study. Therefore, we unavoidably considered those cases as metastatic disease even though there had been only a short interval between the completion of therapy and the development of metastatic disease. In conclusion, patients with the primary tumor in an extremity tended to have metastasis into the LNs. Sixty percent of these patients showed distant metastasis without locoregional recurrence detected during follow-up. Older patient age at initial presentation and unfavorable sites of the primary tumor were factors associated with distant metastasis. Therefore, imaging surveillance should be optimized according to patient age at initial presentation as well as the location of the primary tumor. References 1. Ries L, Smith M, Gurney J, et al. Cancer incidence and survival among children and adolescents: United States SEER Program Bethesda, MD: Surveillance, Epidemiology, and End Results Program, National Cancer Institute, Pappo AS, Anderson JR, Crist WM, et al. Survival after relapse in children and adolescents with rhabdomyosarcoma: a report from the Intergroup Rhabdomyosarcoma Study Group. J Clin Oncol 1999; 17: Lawrence W Jr, Anderson JR, Gehan EA, Maurer H. Pretreatment TNM staging of childhood rhabdomyosarcoma: a report of the Intergroup Rhabdomyosarcoma Study Group. Children s Cancer Study Group. Pediatric Oncology Group. 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Primary and metastatic rhabdomyosarcoma in the breast: neoplasms of adolescent females, a report from the Intergroup Rhabdomyosarcoma Study. Med Pediatr Oncol 1997; 29: D Angelo P, Carli M, Ferrari A, et al. Breast metastases in children and adolescents with rhabdomyosarcoma: experience of the Italian Soft Tissue Sarcoma Committee. Pediatr Blood Cancer 2010; 55: Lin JL, Guillerman RP, Russell HV, Lupo PJ, Nicholls L, Okcu MF. Does routine imaging of patients for progression or relapse improve survival in rhabdomyosarcoma? Pediatr Blood Cancer 2016; 63: FOR YOUR INFORMATION A data supplement for this article can be viewed in the online version of the article at: AJR:209, August 2017
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