Whole-Body MR Imaging for Detection of Bone Metastases in Children and Young Adults: Comparison with Skeletal Scintigraphy and FDG PET
Abstract
OBJECTIVE. The purpose of this study was to compare the diagnostic accuracy of whole-body MR imaging, skeletal scintigraphy, and 18F-fluorodeoxyglucose (FDG) positron emission tomography (PET) for the detection of bone metastases in children.
SUBJECTS AND METHODS. Thirty-nine children and young adults who were 2-19 years old and who had Ewing's sarcoma, osteosarcoma, lymphoma, rhabdomyosarcoma, melanoma, and Langerhans' cell histiocytosis underwent whole-body spin-echo MR imaging, skeletal scintigraphy, and FDG PET for the initial staging of bone marrow metastases. The number and location of bone and bone marrow lesions diagnosed with each imaging modality were correlated with biopsy and clinical follow-up as the standard of reference.
RESULTS. Twenty-one patients exhibited 51 bone metastases. Sensitivities for the detection of bone metastases were 90% for FDG PET, 82% for whole-body MR imaging, and 71% for skeletal scintigraphy; these data were significantly different (p < 0.05). False-negative lesions were different for the three imaging modalities, mainly depending on lesion location. Most false-positive lesions were diagnosed using FDG PET.
CONCLUSION. Whole-body MR imaging has a higher sensitivity than skeletal scintigraphy for the detection of bone marrow metastases but a lower sensitivity than FDG PET.
Introduction
In patients with primary tumors that potentially metastasize to bone, the diagnosis of bone metastasis is crucial to determine the prognosis and to optimize therapy [1, 2]. 99mTc-phosphonate—based skeletal scintigraphy is the standard method for the initial staging of bone tumors. However, it depicts bone metastases at a relatively advanced stage of tumor infiltration when osteoblastic host reaction to tumor deposits has already occurred. In addition, anatomic detail, sensitivity, and specificity are limited [1, 3,4,5,6]. In adults, the sensitivity of skeletal scintigraphy was reported to be about 62-89% [1, 4,5,6,7].
New imaging techniques such as MR imaging and positron emission tomography (PET) can identify bone metastases at an earlier stage of growth, before host reactions of the osteoblasts occur [4, 5]. Whole-body MR imaging has the potential to visualize the bone marrow (the initial site of neoplastic cell infiltration) directly and to determine abnormalities in bone marrow cell composition with high anatomic resolution [6, 8]. Fluorine-18-fluorodeoxyglucose (FDG) PET depicts early malignant bone marrow infiltration because of its early increased glucose metabolism [9]. In adults, both imaging modalities have been reported to provide sensitivity (up to 100%) for detecting bone metastases superior to that of skeletal scintigraphy [1, 4, 6, 9, 10]. However, special diagnostic problems occur in children because of their highly cellular hematopoietic marrow, which may impair the detection of bone marrow metastases [2, 8, 9, 11]. To our knowledge, no study has compared the feasibility of all three imaging modalities for applications in children and young adults.
The goal of this study was to compare the sensitivity of whole-body MR imaging, skeletal scintigraphy, and FDG PET for detecting bone metastases in pediatric patients.
Subjects and Methods
Patients
Thirty-nine children and young adults with primary tumors that potentially metastasize to bone underwent whole-body MR imaging, skeletal scintigraphy, and FDG PET in a random order as an initial staging procedure before or during the first 10 days of chemotherapy. The study was approved by the internal oncology review board. Informed consent was obtained from the parents for each of the three imaging procedures. The patient population included 12 females and 27 males who ranged in age from 2 to 19 years (mean age, 12.9 years). Primary tumors comprised Ewing's sarcoma (n = 20), osteosarcoma (n = 3), rhabdomyosarcoma (n = 3), malignant lymphoma (n = 2), myelosarcoma (n = 1), malignant melanoma (n = 1), and Langerhans' cell histiocytosis (n = 9). Whole-body MR imaging, skeletal scintigraphy, and FDG PET were performed in all patients as part of the pretherapeutic examination. The interval for completion of all three imaging modalities was 3-25 days (mean interval, 11 days).
As a standard of reference, all malignant primary tumors and 22 of the 51 bone metastases were analyzed histopathologically at either open surgery or CT-guided biopsy. This analysis included all bone lesions that were suspicious for metastasis with one imaging modality but not with the other modalities. All bone metastases underwent clinical and imaging follow-up for at least 10 months and for as long as 2 years.
MR Imaging
MR imaging was performed using two 1.5-T systems (Magnetom SP and Magnetom Vision; Siemens, Erlangen, Germany). The patients were placed supine within the smallest available coil; that is, small children were examined with a head coil, and older patients were examined using the body coil. Images of the spine were acquired using a circularly polarized spine coil. Axial T1-weighted spin-echo images were acquired using a TR range/TE of 450-500/15 msec, 2 acquisitions, a field of view of 300-500 mm2, a matrix of 192-256 × 256 pixels, and an effective slice thickness of 4-6 mm. In smaller children, nine slabs with 9-15 slices each were acquired, which included head, thorax, abdomen, upper and lower spine, and the extremities. Slice orientation was coronal for the trunk and extremities and sagittal for the spine (Fig. 1). In adolescents, upper and lower extremities were covered by two slabs each. To include both forearms in one slab, the arms were elevated above the head. The entire MR imaging procedure took 45 min in young children and 55-60 min in older children and adolescents.
In a pilot study, we performed both T1-weighted spin-echo and T2-weighted fat-suppressed short tau inversion recovery (STIR) imaging (TR/TE, 5420/29; flip angle, 180°) in the first 10 patients. In all subsequent patients, we performed spin-echo sequences only because the spin-echo images had a faster acquisition time (4 min per slab as opposed to 8 min per slab for STIR), showed fewer movement artifacts, had a higher spatial resolution, and, as also reported by other investigators [2, 12], had a comparable sensitivity but higher specificity than STIR images in children.
Skeletal Scintigraphy
Standard skeletal scintigraphy was performed using a planar three-phase technique. Whole-body scans were obtained 3-4 hr after the IV injection of 99mTc-labeled methylene diphosphonate with an activity of 740 MBq in adults. In children, activity was adjusted to body weight according to the recommendations of the European Association of Nuclear Medicine Pediatric Task Group [13]. Images were acquired using a whole-body scanner (Body-Scan; Siemens) with a low-energy, high-resolution collimator at a speed of 15 cm/min. Additionally, SPECT (single photon emission computed tomography) was performed in case of equivocal bone lesions on conventional bone scans.
PET
PET was performed with FDG. Before the FDG PET examinations, all patients fasted for at least 5 hr. No patient had diabetes or pathologic glucose tolerance, and blood glucose levels were confirmed to be less than 6.7 mmol/L immediately before the radionuclide injection. In addition, all patients received 5 mg of diazepam orally about 1 hr before the FDG injection in order to provide muscle relaxation. FDG was injected at a rate of 3.7 MBq/kg of body weight, followed by an IV administration of 500 mL of 0.9% saline solution at a rate of approximately 17 mL/min and a subsequent IV injection of 1 mg/kg of body weight of furosemide (maximum, 20 mg). The urinary bladder was emptied. In all patients, whole-body emission scans (6-8 bed positions) were obtained about 60 min after the FDG injection using an ECAT EXACT 921/47 PET camera (CTI/Siemens, Knoxville, TN), which allows simultaneous acquisition of 47 continuous images with a thickness of 3.375 mm each. Images were reconstructed by filtered back-projection with a Butterworth (0.5) filter. In the last nine patients, emission and transmission scans (6 min and 4 min per bed position) were obtained. Attenuation correction images were reconstructed iteratively. Additionally, emission images without attenuation correction were created by filtered back-projection.
Data Analysis
Qualitative image evaluation was performed by four reviewers with reference to individual patients and individual lesions: MR images were analyzed in consensus by two experienced radiologists, and skeletal scintigrams and FDG PET images were analyzed separately by two experienced nuclear medicine physicians. Reviewers were unaware of the results of the other imaging modalities. Clinical data such as primary tumor, age, and sex of the patient and status before or at the beginning of chemotherapy were available to all reviewers. For all imaging modalities, lesion number and location were determined. In three patients with diffuse bone marrow metastases, a maximum of five bone lesions per patient were included in the lesion-by-lesion analysis. In addition, the approximate lesion size was measured on the basis of the whole-body MR image or additional MR scans of the region. In cases of lesions not seen on MR imaging, the approximate lesion size was estimated using the other imaging techniques. After completion of data analyses, all reviewers and the oncologist responsible for the patient compared the findings of the three imaging techniques. Equivocal bone lesions were further evaluated by biopsy, additional imaging, or follow-up studies.
On T1-weighted spin-echo images, a metastatic bone or bone marrow lesion was defined as focal or diffuse hypointense bone marrow signal intensity relative to adjacent (or, in the extremities, contralateral) normal bone marrow. In patients older than 10 years, normal bone marrow was defined as hyperintense relative to adjacent skeletal muscle tissue, and neoplastic marrow was defined as hypo- or isointense to adjacent muscle tissue. In younger patients, the distribution of normal hematopoietic marrow as previously shown by Kricun [14] and Moore and Dawson [15] was considered in the assessment. With skeletal scintigraphy or FDG PET, a metastatic bone lesion was defined as an area of focal increased radionuclide uptake relative to adjacent and contralateral normal tissue not located in a region of physiologically increased uptake.
The number of detected bone metastases was summarized in frequency tables. The diagnoses made by the reviewers were characterized as true-positive, false-negative, and false-positive. For each imaging modality, sensitivity was calculated using the following equation: sensitivity (%) = (true-positives / true-positives + false-negatives) × 100. Specificity could not be calculated because true-negatives could not be accurately defined. Statistical significance of differences between data of the three imaging modalities was tested using the McNemar test, with a p value of less than 0.05 considered significant.
Results
With analysis on a patient-by-patient basis, 18 of the 39 examined patients showed no metastases at clinical and imaging follow-up for at least 10 months. These 18 patients were correctly diagnosed as true-negative with MR imaging or skeletal scintigraphy, but two of these patients showed false-positive lesions with FDG PET (Table 1). According to the standard of reference, 21 patients showed bone metastases. Sixteen of these 21 patients were correctly identified as true-positive by MR imaging and skeletal scintigraphy, and 18 patients were correctly identified with FDG PET, signifying a significantly higher sensitivity for FDG PET (86%) than for either MR imaging (76%) or skeletal scintigraphy (76%) (p < 0.05; Table 1).
| Category | No. of Patients (n = 39) | No. of Lesions (n = 51) | ||||
|---|---|---|---|---|---|---|
| MRI | SSC | PET | MRI | SSC | PET | |
| True-negative | 18 | 18 | 16 | NA | NA | NA |
| True-positive | 16 | 16 | 18 | 42 | 36 | 46 |
| False-negative | 5 | 5 | 3 | 9 | 15 | 5 |
| False-positive | 0 | 0 | 2 | 3 | 3 | 6 |
| Sensitivity (%) | 76 | 76 | 86 | 82 | 71 | 90 |
| Note.—The gold standard was histopathology and clinical and imaging follow-up wherein 18 patients had negative findings for metastases and 21 patients had positive findings. NA = not applicable. | ||||||
The 21 patients with bone metastases exhibited a total of 51 focal bone lesions, proven either by bone biopsy or imaging follow-up. With analysis on a lesion-by-lesion basis, whole-body MR imaging showed a sensitivity of 82% for the detection of bone metastases, which was significantly higher than the sensitivity of 71% for skeletal scintigraphy (p < 0.05; Table 1) but significantly lower than the sensitivity of 90% for FDG PET (p < 0.05; Table 1). As shown in Table 2, most true-positive bone lesions were diagnosed in patients with Ewing's sarcoma and Langerhans' cell histiocytosis. In one patient with osteosarcoma, a single metastasis was diagnosed on skeletal scintigraphy and MR imaging but not on FDG PET. In one patient with malignant non-Hodgkin's lymphoma, bone infiltration was depicted on all three imaging modalities. In all other primary tumors and in patients with histiocytosis, whole-body MR imaging and FDG PET detected more bone metastases than skeletal scintigraphy (Table 2).
| Primary Tumor | MR Imaging | SSC | PET | Totala |
|---|---|---|---|---|
| Ewing's sarcoma | 20 | 20 | 22 | 25 |
| Osteosarcoma | 1 | 1 | 0 | 1 |
| Lymphoma | 1 | 1 | 1 | 1 |
| Rhabdomyosarcoma | 5 | 4 | 6 | 6 |
| Malignant melanoma | 4 | 2 | 4 | 4 |
| Langerhans' cell histiocytosis | 11 | 8 | 13 | 14 |
| Total | 42 | 36 | 46 | 51 |
| Note.—SSC = skeletal scintigraphy, PET = positron emission tomography. | ||||
a
As determined by the standard of reference, which was clinical and imaging follow-up for at least 10 months after completion of the study or histopathology.
Bone metastases that were not diagnosed with each imaging technique were different and depended on lesion location (Table 3). Most false-negative findings with MR imaging were located in small or flat bones of the ribs (n = 3), the skull (n = 2), the distal radius (n = 1), or the carpal bone (n = 1) (Table 3 and Fig. 2A,2B,2C). Skeletal scintigraphy showed most false-negative lesions in the spine (n = 9) (Table 3 and Fig. 3A,3B,3C). With FDG PET, most false-negative lesions were located in the skull (n = 3) (Table 3 and Fig. 4A,4B,4C).
| Location | MR Imaging | SSC | PET | Totala |
|---|---|---|---|---|
| Upper extremity | 4 | 5 | 6 | 6 |
| Lower extremity | 13 | 10 | 12 | 13 |
| Spine | 10 | 3 | 12 | 12 |
| Skull | 4 | 6 | 3 | 6 |
| Thorax | 4 | 6 | 7 | 7 |
| Pelvis | 7 | 6 | 6 | 7 |
| Total | 42 | 36 | 46 | 51 |
| Note.—SSC = skeletal scintigraphy, PET = positron emission tomography. | ||||
a
As determined by the standard of reference, which was clinical and imaging follow-up for at least 10 months after completion of the study or histopathology.
The number of detected bone lesions was inversely related to lesion size for all imaging modalities. Large lesions with a diameter greater than 5 cm were correctly diagnosed with whole-body MR imaging and FDG PET in 100% (15/15) of patients and with skeletal scintigraphy in 93% (14/15). A diffuse infiltration of the spine was missed with skeletal scintigraphy in one patient. Smaller lesions with diameters of 1-5 cm were correctly diagnosed with whole-body MR imaging in 79% (23/29) of patients, with skeletal scintigraphy in 62% (18/29), and with FDG PET in 86% (25/29). Bone metastases with diameters smaller than 1 cm were correctly diagnosed with whole-body MR imaging in 57% (4/7) of patients, with skeletal scintigraphy in 57% (4/7), and with FDG PET in 86% (6/7) (Table 4).
| Lesion Size | MR Imaging | SSC | PET | Totala |
|---|---|---|---|---|
| <1 cm | 4 | 4 | 6 | 7 |
| 1-5 cm | 23 | 18 | 25 | 29 |
| <5 cm | 15 | 14 | 15 | 15 |
| Total | 42 | 36 | 46 | 51 |
| Note. —SSC = skeletal scintigraphy, PET = positron emission tomography. | ||||
a
As determined by MR imaging or (in cases not seen on MR imaging) estimated on the basis of conventional radiography, CT, or surgical findings.
Most false-positive bone lesions were found with FDG PET, including focal areas of increased FDG uptake in the humerus (n = 2), tibia (n = 2; Fig. 5A,5B,5C), and femur (n = 2). These lesions were not shown with any other imaging modalities or with imaging or clinical follow-up. With MR imaging, three false-positive benign bone lesions were detected, including one simple bone cyst, one enchondroma, and one osteoma. The latter two were also diagnosed with skeletal scintigraphy. In addition, skeletal scintigraphy depicted a sclerotic nonossified fibroma that showed only cortical thickening on MR imaging and was not diagnosed as suspected of being a malignant lesion. Neither MR imaging nor skeletal scintigraphy showed false-positive findings in the absence of pathologic findings.
Combining two imaging modalities, sensitivities for lesion detection were 90% (46/51) for skeletal scintigraphy and MR imaging, 96% (49/51) for skeletal scintigraphy and FDG PET, and 96% (49/51) for MR imaging and FDG PET. Thus, the sensitivities of skeletal scintigraphy (71%) and MR imaging (82%) alone were significantly increased either by combination with each other or by combination with FDG PET (p < 0.05). However, the sensitivity of FDG PET (90%) was not significantly increased by combination with one of the other imaging modalities (p > 0.05).
Discussion
In this study, both whole-body MR imaging and FDG PET showed a higher sensitivity than standard skeletal scintigraphy for the detection of bone metastases in children and young adults. The pathologic basis for these findings is the initial accumulation of hematogenously seeded tumor cells in the intramedullary compartment, leading to replacement of the normal hematopoietic marrow and tumor cell proliferation before reactive osteoblastic responses occur [4, 5, 16]. MR imaging directly reveals increased T1 and T2 relaxation times of neoplastic bone marrow infiltrates [6, 8, 16]. FDG PET directly depicts the increased glucose metabolism of neoplastic cells in the bone marrow [9].
Alternative screening modalities, such as conventional radiography and CT, for the detection of bone marrow metastases have been shown to be less sensitive than skeletal scintigraphy [11, 16, 17]. Bone marrow scintigraphy showed a higher sensitivity for the detection of bone marrow metastases than skeletal scintigraphy [18], but the radiation exposure on bone marrow scintigraphy would be too great for routine staging in children.
Different lesions were missed with the three imaging modalities, emphasizing a complementary role of these methods for tumor staging and indicating potential technical and diagnostic problems with each modality.
With whole-body MR imaging, technical problems arise as a result of relatively long examination times (45-60 min) and limited depiction of metastases in small bones [6, 8, 19]. However, the development of ultrafast pulse sequences for whole-body MR imaging may decrease the imaging time substantially [6, 20]. Using new echoplanar imaging techniques, 180 contiguous axial images can be obtained from the cranial vertex through the feet in 6 min [21]. Additionally, new three-dimensional pulse sequences may improve spatial resolution and allow reformations of flat bones such as ribs.
In children, special diagnostic problems occur with the differentiation of highly cellular hematopoietic marrow and neoplasia, requiring knowledge of age-dependent conversion patterns from hematopoietic to fatty bone marrow [14, 15, 22, 23]. The differentiation between highly cellular hematopoietic and neoplastic marrow may be facilitated by in-phase and out-of-phase pulse sequences, which display both entities with different signals, and by reticuloendothelial system—specific contrast agents, which reduce the signal intensity of hematopoietic macrophage-containing marrow but not of neoplastic marrow [24, 25].
Skeletal scintigraphy provides limited spatial resolution and limited specificity, requiring further imaging to characterize regions of abnormal radionuclide uptake [6, 10]. Diagnostic problems in children may arise because of the high osteoblastic activity of epiphyseal plates, which could superimpose bone lesions. Additional SPECT examinations can improve sensitivity, especially in the spine [16]. In this study, SPECT was added in cases of suspected or equivocal bone lesions on planar scintigraphy. SPECT is not performed routinely when planar scintigraphy reveals normal findings.
FDG PET also has a limited spatial resolution and requires complementary CT or MR imaging to localize an area of increased glucose metabolism. Moreover, FDG PET shows a high number of false-positive lesions in this and other studies, and these lesions have to be followed up with other imaging modalities [26, 27]. Adding semiquantitative criteria for FDG tumor uptake to qualitative image evaluations may increase specificity [28]. Another problem with FDG PET is the identification of skull metastases, because normal brain exhibits a high glucose metabolism, which may obscure metastases [28].
Tumor metabolism and, consequently, tumor detection with FDG PET may be highly susceptible to chemotherapy. In this study, two patients who underwent FDG PET after the initiation of chemotherapy had false-negative findings for metastases. The primary tumors in these patients also showed response to therapy. However, these findings did not affect our study results significantly. Staging with FDG PET before any therapy is difficult to organize, because PET is usually not available on a day-by-day basis. Thus, in some instances FDG PET must be performed after the initiation of therapy; otherwise, it may delay the start of therapy. This problem would not arise with other imaging modalities: skeletal scintigraphy and MR imaging are more widely available, usually on a day-by-day basis in cancer centers. In addition, skeletal scintigraphy shows a slowly reduced or even increased radionuclide uptake by bone metastases with response to chemotherapy [6, 29], and MR imaging shows a delayed reduction in tumor size and contrast enhancement with chemotherapy [15, 22]. Future studies are needed to show how quickly FDG PET depicts tumor response to chemotherapy and whether FDG PET performed within the first days after initiation of chemotherapy has reduced sensitivity.
With respect to economic constraints, the financial impact of a staging modality has to be considered. At our institution, standard skeletal scintigraphy is the most inexpensive imaging test. For comparison, costs for whole-body MR imaging are about two to three times higher, and costs for FDG PET are even eight times higher, than costs for skeletal scintigraphy. As an alternative to FDG PET, considering costs and its limited availability, our data show that combined whole-body MR imaging and skeletal scintigraphy are less expensive but lead to a comparable sensitivity.
Conclusions must be limited to the scope of the study. Data have been acquired in young patients; findings may be different in older patients with different bone marrow cell compositions, different malignant primary tumors, and different growth patterns of bone marrow metastases. To our knowledge, ours is the first comparative study of whole-body MR imaging, skeletal scintigraphy, and FDG PET in children and young adults. The study population has a wide spectrum of disorders, all of which are rare. Bone metastases in these primary tumors are even more rare. Further studies may be required in patients with more homogenous tumor groups. However, such studies may require a multicenter approach. We did not include children with neuroblastomas in our study because those patients would have to be examined under general anaesthesia and the approach of scintigraphic staging is different than for other patients in this study. We included patients with Langerhans' cell histiocytosis, although skeletal scintigraphy has a well-known low sensitivity for lesion detection in this disease. However, our data show that whole-body MR imaging and FDG PET are alternative staging methods with improved sensitivity. Because whole-body MR imaging does not expose the patient to irradiation, our clinicians accept this new technique, especially for patients with benign disease.
Whole-body MR imaging was performed with high-magnetic-field (1.5 T) MR scanners, and findings must be proven with lower field strengths. In this study, whole-body MR imaging was performed using T1-weighted spin-echo images, although STIR images have been described as being more sensitive in adults [5]. In children, however, we found, in agreement with others, fewer false-positive lesions on spin-echo images than on STIR images [2, 12]. The highly cellular hematopoietic marrow in children may cause a diffuse or even focal and asymmetric increased bone marrow signal intensity on STIR images, which may impair bone marrow lesion detection and decrease the specificity of that method. Additionally, small children often display a nonspecific increased bone marrow signal intensity in the lower limbs, which may be the result of minor bone bruises [12, 15, 22]. These findings are only subtle on spin-echo images and usually produce few problems for the differential diagnosis.
In summary, new imaging techniques such as whole-body MR imaging and FDG PET may improve the detection of bone and bone marrow metastases in children and adolescents compared with standard skeletal scintigraphy. Optimized staging procedures may be lifesaving through the early detection of metastases and through early imaging-based treatment planning [11, 21, 29]. New techniques such as ultrafast whole-body MR imaging and PET with tumor-specific tracers may further improve detection and characterization of bone lesions, leading to individually optimized local and systemic therapies. Our data encourage further investigation and technical optimization of whole-body MR imaging and FDG PET for the detection of bone and bone marrow metastases in pediatric patients.
Footnotes
Supported by German Cancer Research Foundation grant (Mildred Scheel Stiftung) D/96/17149, no. 683 400 001.
Address correspondence to H. E. Daldrup-Link.
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Submitted: September 18, 2000
Accepted: December 22, 2000
First published: November 23, 2012
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