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False-Positive Findings on 18F-FDG PET/CT: Differentiation of Hibernoma and Malignant Fatty Tumor on the Basis of Fluctuating Standardized Uptake Values

¹ Department of Radiology and Nuclear Medicine, Memorial Sloan Kettering Cancer Center, 1275 York Ave., New York, NY 10021.
² Department of Pathology, Memorial Sloan-Kettering Cancer Center, New York, NY.

Received January 6, 2007; accepted after revision October 29, 2007.

 
Address correspondence to C. S. Smith.

Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
OBJECTIVE. Hibernoma is a benign tumor of brown fat that has imaging features similar to those of malignant fat-containing soft-tissue tumors. Hibernoma is metabolically active on ¹⁸F-FDG PET/CT, and its presence can lead to false-positive interpretations. We present three cases in which fatty lesions with increased radiotracer uptake identified on FDG PET/CT turned out to be hibernomas. The standardized uptake values of the lesions were similar to those reported in the literature for liposarcoma. However, all three patients had variable standardized uptake values over time.

CONCLUSION. Variation in standardized uptake values over time is an imaging characteristic that may be helpful for differentiating hibernoma and malignant fatty tumor.

Keywords: hibernoma • liposarcoma • PET/CT

Introduction

Top Abstract Introduction Materials and Methods Results Discussion References

 
PET/CT with ¹⁸F-FDG is routinely used in the staging and restaging of various malignant tumors. It is well recognized that many false-positive results occur in interpretation of the scans. One common false-positive finding on FDG PET is radiotracer uptake within brown fat. Hibernoma is a benign but metabolically active tumor of brown fat origin that can have cross-sectional imaging characteristics similar to those of other fat-containing tumors, such as lipoma and liposarcoma. To date there have been three case reports [1–3] to our knowledge of intense uptake of FDG in hibernoma. Some of the authors concluded that the standardized uptake values (SUVs) of FDG PET can be used to differentiate hibernoma from fatty sarcomas, such as liposarcoma, which have lower SUVs. It has also been reported that FDG PET is useful in differentiating tumor grades of soft-tissue sarcomas, including liposarcoma [4], on the basis of SUV measurements.

We present the three cases in which the diagnosis of hibernoma was made when the SUVs were similar to those reported for liposarcoma and other soft-tissue tumors [4–6]. Hibernomas therefore are benign tumors that can result in a false-positive interpretation by exhibiting increased FDG activity with an SUV similar to that of liposarcoma. In our small series, we noticed that the FDG activity within these tumors fluctuated over time without any type of intervention. This finding may be a helpful feature for differentiating these benign tumors from malignant fatty tumors.

Materials and Methods

Top Abstract Introduction Materials and Methods Results Discussion References

 
Between August 2003 and September 2005, a retrospective review of all routine oncology FDG PET/CT studies performed at our institution revealed the records of three patients with the ultimate diagnosis of hibernoma. The patients were two men and one woman 54, 55, and 82 years old. The institutional review board approved a retrospective review of each patient's notes and images.

Patients were given a standard-activity IV injection of 15 mCi (555 MBq) of FDG, and images were acquired after a 45- to 60-minute uptake period. Low-dose unenhanced CT and PET images were acquired with a dedicated PET/CT scanner (Biograph LSO, Siemens Medical Solutions/CTI, or Discovery LS, GE Healthcare). The field of view extended from at least the skull base to at least the inguinal regions, depending on the clinical question. Parameters for low-dose CT were slice thickness, 5 mm; 120 kVp; tube current, 110 mA. PET, CT, and fusion images were reviewed on a workstation integrated with a PACS (Advantage, GE Healthcare). This system allowed reformatting of images with display of transaxial, coronal, and sagittal slices and calculation of SUV with placement of a volumetric region of interest around the structure of interest.

PET and CT images were first analyzed visually. FDG uptake outside normal anatomic structures and with an intensity greater than background activity in a mass that had fatty components on CT and was thought to be hibernoma was noted. The maximum SUV, corrected for body weight, within a given region of interest also was recorded and was confirmed on fusion images. The CT attenuation of the mass was recorded. When available, contrast-enhanced CT and MR images obtained within 2 weeks of PET/CT were reviewed for further evaluation of PET/CT findings. Patho logic results were available in one case, and the gross and microscopic slides of the surgical specimen were reviewed by a pathologist. Clinical notes, including those on follow-up images of the two patients who had FDG uptake in a fatty mass thought to represent hibernoma and who did not undergo biopsy, were reviewed for lesion stability.

View larger version (105K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A —82-year-old woman with newly diagnosed lymphoma. Coronal (A) and axial (B) PET, axial CT (C), and fusion axial PET/CT (D) images from staging 18F-FDG PET/CT show hypermetabolic enlarged spleen and right retroperitoneal adenopathy (white arrows, B–D) and small focus of increased activity in left paraspinal region (black arrow).

View larger version (98K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B —82-year-old woman with newly diagnosed lymphoma. Coronal (A) and axial (B) PET, axial CT (C), and fusion axial PET/CT (D) images from staging 18F-FDG PET/CT show hypermetabolic enlarged spleen and right retroperitoneal adenopathy (white arrows, B–D) and small focus of increased activity in left paraspinal region (black arrow).

View larger version (107K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C —82-year-old woman with newly diagnosed lymphoma. Coronal (A) and axial (B) PET, axial CT (C), and fusion axial PET/CT (D) images from staging 18F-FDG PET/CT show hypermetabolic enlarged spleen and right retroperitoneal adenopathy (white arrows, B–D) and small focus of increased activity in left paraspinal region (black arrow).

View larger version (108K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1D —82-year-old woman with newly diagnosed lymphoma. Coronal (A) and axial (B) PET, axial CT (C), and fusion axial PET/CT (D) images from staging 18F-FDG PET/CT show hypermetabolic enlarged spleen and right retroperitoneal adenopathy (white arrows, B–D) and small focus of increased activity in left paraspinal region (black arrow).

View larger version (80K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1E —82-year-old woman with newly diagnosed lymphoma. Coronal (E) and axial (F) PET, axial CT (G), and fusion axial PET/CT (H) images from FDG PET/CT performed after four cycles of rituximab, vincristine, doxorubicin, cyclophosphamide, and prednisone (R-CHOP) therapy show resolution of activity in spleen and retroperitoneum and increase in activity in left paraspinal region (arrow). Biopsy result was hibernoma.

View larger version (89K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1F —82-year-old woman with newly diagnosed lymphoma. Coronal (E) and axial (F) PET, axial CT (G), and fusion axial PET/CT (H) images from FDG PET/CT performed after four cycles of rituximab, vincristine, doxorubicin, cyclophosphamide, and prednisone (R-CHOP) therapy show resolution of activity in spleen and retroperitoneum and increase in activity in left paraspinal region (arrow). Biopsy result was hibernoma.

View larger version (82K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1G —82-year-old woman with newly diagnosed lymphoma. Coronal (E) and axial (F) PET, axial CT (G), and fusion axial PET/CT (H) images from FDG PET/CT performed after four cycles of rituximab, vincristine, doxorubicin, cyclophosphamide, and prednisone (R-CHOP) therapy show resolution of activity in spleen and retroperitoneum and increase in activity in left paraspinal region (arrow). Biopsy result was hibernoma.

View larger version (97K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1H —82-year-old woman with newly diagnosed lymphoma. Coronal (E) and axial (F) PET, axial CT (G), and fusion axial PET/CT (H) images from FDG PET/CT performed after four cycles of rituximab, vincristine, doxorubicin, cyclophosphamide, and prednisone (R-CHOP) therapy show resolution of activity in spleen and retroperitoneum and increase in activity in left paraspinal region (arrow). Biopsy result was hibernoma.

View larger version (124K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1I —82-year-old woman with newly diagnosed lymphoma. Photomicrograph of biopsy specimen from left paraspinal mass shows benign adipose cells of brown fat type. Cells have distinct cell borders with multiple vacuoles in cytoplasm or eosinophilic granular cytoplasm with areas composed of mature adipose tissue. (H and E, x40)

View larger version (90K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A —54-year-old man with increasing level of prostate-specific antigen after radical prostatectomy. Coronal PET images from serial 18F-FDG PET/CT show focus of increased activity in fatty-appearing lesion adjacent to left teres major muscle (arrow, B and C). Standard uptake value fluctuates over time from no uptake (A) through 6.7 approximately 1 month later (B) to 5.0 3 months after that (C).

View larger version (84K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B —54-year-old man with increasing level of prostate-specific antigen after radical prostatectomy. Coronal PET images from serial 18F-FDG PET/CT show focus of increased activity in fatty-appearing lesion adjacent to left teres major muscle (arrow, B and C). Standard uptake value fluctuates over time from no uptake (A) through 6.7 approximately 1 month later (B) to 5.0 3 months after that (C).

View larger version (82K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C —54-year-old man with increasing level of prostate-specific antigen after radical prostatectomy. Coronal PET images from serial 18F-FDG PET/CT show focus of increased activity in fatty-appearing lesion adjacent to left teres major muscle (arrow, B and C). Standard uptake value fluctuates over time from no uptake (A) through 6.7 approximately 1 month later (B) to 5.0 3 months after that (C).

View larger version (62K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2D —54-year-old man with increasing level of prostate-specific antigen after radical prostatectomy. Axial contrast-enhanced CT scan obtained 20 months after A–C shows stability in both size and appearance of fatty lesion adjacent to left teres major muscle (arrow).

Top Abstract Introduction Materials and Methods Results Discussion References

The second case was that of a 54-year-old man who underwent radical prostatectomy and pelvic lymph node resection for Gleason grade 8 (4 + 4) prostate cancer (Figs. 2A, 2B, 2C, and 2D). Pathologic examination showed extensive extracapsular extension and positive results for tumor in one of seven left pelvic lymph nodes. One year after surgery, the patient underwent FDG PET/CT as part of a research protocol before beginning hormonal and taxane-based chemotherapy. No abnormal FDG activity was identified at that time. Approximately 1 month later, FDG PET/CT showed increased FDG activity (SUV, 6.7) within a fatty-appearing lesion (attenuation, –48 H) beside the left teres major muscle. Follow-up PET/CT at 3 months showed a decrease in activity (SUV, 5.0) within the lesion without any type of intervention. CT performed 18 months later showed no change in the size of the lesion.

In the third case, a 55-year-old man underwent FDG PET/CT for evaluation of extent of disease after low anterior resection for colorectal carcinoma (Figs. 3A, 3B, 3C, 3D, and 3E). PET/CT showed multiple hypermetabolic hepatic metastatic lesions and incidentally showed increased uptake (SUV, 5.0) in the left flank deep in relation to the left latissimus dorsi muscle. This area of uptake corresponded to a lesion with low attenuation (–71 H) consistent with that of fat. The patient started intraarterial hepatic chemotherapy with irinotecan, and PET/CT performed 3 months later showed interval resolution of the activity within the liver but an increase in activity (SUV, 11) within the left flank. The size of the lesion had not increased on the CT component. CT performed 2 years later showed that the size of the lesion had decreased.

View larger version (82K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A —55-year-old man with newly diagnosed colorectal cancer. Coronal (A) and axial (B) PET, axial CT (C), and fusion axial PET/CT (D) images from 18F-FDG PET/CT show increased FDG activity within numerous hepatic metastatic lesions (white arrow). Focus of increased activity deep in relation to left latissimus dorsi muscle within fatty-appearing lesion (black arrow) suggests hibernoma.

View larger version (76K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B —55-year-old man with newly diagnosed colorectal cancer. Coronal (A) and axial (B) PET, axial CT (C), and fusion axial PET/CT (D) images from 18F-FDG PET/CT show increased FDG activity within numerous hepatic metastatic lesions (white arrow). Focus of increased activity deep in relation to left latissimus dorsi muscle within fatty-appearing lesion (black arrow) suggests hibernoma.

View larger version (106K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C —55-year-old man with newly diagnosed colorectal cancer. Coronal (A) and axial (B) PET, axial CT (C), and fusion axial PET/CT (D) images from 18F-FDG PET/CT show increased FDG activity within numerous hepatic metastatic lesions (white arrow). Focus of increased activity deep in relation to left latissimus dorsi muscle within fatty-appearing lesion (black arrow) suggests hibernoma.

View larger version (105K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3D —55-year-old man with newly diagnosed colorectal cancer. Coronal (A) and axial (B) PET, axial CT (C), and fusion axial PET/CT (D) images from 18F-FDG PET/CT show increased FDG activity within numerous hepatic metastatic lesions (white arrow). Focus of increased activity deep in relation to left latissimus dorsi muscle within fatty-appearing lesion (black arrow) suggests hibernoma.

View larger version (119K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3E —55-year-old man with newly diagnosed colorectal cancer. Axial contrast-enhanced CT scan obtained 12 months after chemotherapy shows decrease in size of hepatic metastatic lesions and decrease in size of fatty lesion deep in relation to left latissimus dorsi muscle.

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
Two types of adipose tissue are present in the body: white adipose tissue, which acts as insulation and an energy depot, and brown adipose tissue, which has the ability to generate heat in response to cold exposure (nonshivering thermogenesis) and ingestion of food (diet thermogenesis) [7]. Brown fat is found most commonly in the neck, chest near large blood vessels, axillae, perinephric region, and intercostal spaces and along the spine and paraaortic muscles [8, 9]. It is present in neonates, but the amount decreases with age. Because it as a major producer of heat and contains a large number of mitochondria, brown fat is highly metabolic, and intense increased uptake of FDG in areas of brown fat can be seen. Yeung at al. [10] found that 3.7% of patients had uptake in areas of brown fat, the SUV ranging from 1.9 to 20. One of the characteristics of brown fat is its variability over time, that is, it can be intense one day and be absent 2 weeks later. The most acceptable theory is related to ambient temperature. A study [11] showed that the incidence of FDG uptake in brown fat increases during cooler periods of the year. Another study [12] showed that controlling a patient's environmental temperature before injection of the radiotracer and during the uptake phase can markedly reduce FDG uptake in areas of brown fat.

Hibernoma, so named because it mimics the brown fat of hibernating animals, is a rare benign tumor of brown fat. It usually manifests as a slowly growing progressively enlarging painless mass. It once was thought that the most common site was residual areas of brown fat. Review of the soft-tissue registry of the Armed Forces Institute, however, showed that the most common location was the thigh, 30% of cases occurring there [13]. The review also showed a slight male predominance, although hibernomas have been classically described in the literature as being more common among women. The investigators [13] described a number of subsets of hibernoma, the most common of which was typical hibernoma (82% of cases). Other subtypes included eosinophilic, lipoma-like, myxoid, and spindle cell hibernoma. Although there was a difference in the clinicopathologic findings, all variants followed a benign course. At gross inspection, the tumors are well circumscribed, partially encapsulated, and lobulated. Microscopic examination shows all the tumors have multivacuolated fat cells with a small central nucleus to different degrees depending on the subtype.

The radiographic appearance of hibernoma is a radiolucent mass without bony involvement. The masses are often heterogeneous on MRI and CT with characteristics similar but not identical to those of fat. Hibernoma can contain internal septations or fine enhancing strands, and often a dominant vessel is identified within the lesion after administration of IV contrast material. The finding of a large branching vessel within a fatty-appearing lesion is strongly suggestive of hibernoma [14]. The differential diagnosis includes liposarcoma and lipoma. Other lesions to consider are angiolipoma, hemangiolipoma, and hemangiopericytoma. Despite the presence of certain imaging features characteristic of hibernoma, pathologic examination often is necessary for diagnosis.

Liposarcoma is one of the most common malignant neoplasms of soft tissue. The age range of persons with this tumor is 40–60 years. The histologic features range from well-differentiated lipoma-like characteristics to extremely pleomorphic neoplasia. Features such as the presence of more than 25% nonadipose tissue favor a diagnosis of liposarcoma [15], but CT and MRI findings are not reliable for distinguishing well-differentiated liposarcoma from benign fatty tumor. In a series of 57 patients, Suzuki et al. [5] evaluated FDG uptake within fatty tumors. They found that benign tumors such as lipoma exhibited no increased uptake and that liposarcomas exhibited increased uptake, the SUV ranging from 0.1 to 6.0, depending on the grade of the tumor.

At least one case of hibernoma with increased uptake (SUV, 20) on ^99mTc tetrofosmin and FDG PET, falsely indicating malignant potential, has been reported [1]. Lin et al. [2] also reported intense uptake (SUV, 20) within a lesion in the gluteus muscle that preoperatively was thought to be myxoid liposarcoma. The lesions was resected, and the pathologic finding was hibernoma. Tsuchiya et al. [3] described two cases of intense FDG activity within two hibernomas in which the SUVs were 11.9 and 26.7. Those authors suggested that because these values were higher than the SUVs previously reported in published studies of liposarcoma, it may be possible to differentiate hibernoma from liposarcoma.

In our case of biopsy-proven hibernoma, the SUV of the lesion initially was 2.7. On follow-up imaging the SUV increased to 4.2, which is in the range reported for liposarcoma. Therefore, in our patients (all of whom had SUVs less than 11) it was not possible to differentiate hibernoma from liposarcoma on the basis of SUV alone. In the cases of the two patients who did not undergo biopsy, the clinical history and lesion characteristics on cross-sectional images were evaluated. Because both patients had no symptoms and the lesions were stable on other images, it was decided not to biopsy the area.

One imaging feature in all of our cases was a fluctuating SUV over time. For example, in the case of the 54-year-old man, no uptake was initially seen in a fatty mass adjacent to the left scapula. One month later, increased FDG uptake (SUV, 6.7) was identified in the same lesion. Approximately 3 months later, the SUV of the lesion had decreased to 5.0. The variables that can affect SUV were comparable for all three scans. For example, the time between injection of the radiotracer and scanning was 1 hour (the SUV of the liver was similar both qualitatively and quantitatively for the three scans), so the differences in SUV were not attributable to differences in uptake period. Because the lesion had variable SUVs over time and the CT findings were of a simple fatty lesion, a decision not to biopsy the lesion was made in this case and in the case of the 55-year-old man. A diagnosis of hibernoma was made (white fat has never been reported to be FDG avid), and follow-up imaging at 18 months in both cases showed a stable lesion in the 54-year-old man and an interval decrease in size of the lesion in the 55-year-old man. This phenomenon of fluctuating SUVs is similar to the pattern we see with FDG uptake in brown fat, which is likely related to differences in ambient temperature. Of note, the 54-year-old patient was being treated with hormonal and taxane-based chemotherapy at the time of the second and third PET scans. In the 55-year-old patient, the SUV of the lesion increased from 5 on the first PET scan to 11 on the second scan. The patient was receiving intraarterial chemotherapy at the time of the second scan.

We acknowledge that treatment might have affected the SUVs. Because, however, the SUVs of the lesions increased and then decreased during the same treatment, and as far as we know there are no literature reports suggesting that FDG uptake in hibernoma or brown fat is affected by chemotherapy, we suggest that this fluctuation is more likely due to differences in ambient temperature. We suggest that this imaging characteristic of hibernoma on FDG imaging may be used to differentiate hibernoma from liposarcoma if confirmed in larger studies. Although we have no hard data of the constancy of SUVs in liposarcoma and we acknowledge this factor as a potential bias, to our knowledge no reports have suggested fluctuation without any form of intervention in malignant neoplasms in general and liposarcoma in particular. This topic has potential for further research.

Interestingly, none of the three patients had increased FDG uptake in other areas of brown fat. One possible explanation for nonvisualization of brown fat at other sites is that there was simply no brown fat in any other areas. Evidence so far suggests that brown fat is found in a minority of patients and is especially rare in adults. Another explanation may be that hibernoma metabolism may be different from metabolism of brown fat and is not subject to normal physiologic regulation, as is normal brown fat.

One limitation of our study was that only one of the patients had a pathologic diagnosis of hibernoma. When all the imaging characteristics in the two other cases were reviewed, it was believed that a diagnosis of hibernoma could be made without histologic proof. This diagnosis was confirmed on follow-up imaging with the findings that the size of the lesions had not increased and that the SUV had decreased or remained stable. Another potential bias of our study was the time between injection of the radiotracer and acquisition of the scans, which can affect SUV measurements. In our three cases, all scans were obtained 45–60 minutes after injection of the radiotracer. In the reported cases of FDG uptake in liposarcoma [2, 5, 6], the time to scanning after injection ranged from 15 to 40 minutes.

Hibernoma is a rare fatty benign tumor that can present incidentally with increased FDG uptake on PET. Radiologists or nuclear medicine physicians reading FDG PET/CT scans should be aware of this entity. In our series all of the lesions had SUVs that overlapped with those reported for liposarcoma, and differentiation of the two entities on the basis of one SUV measurement was not possible. However, all of the patients had fluctuating SUVs over time. If confirmed in larger studies, this imaging feature may be useful for differentiating hibernoma and malignant fatty tumor.

References

Top Abstract Introduction Materials and Methods Results Discussion References

 

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This Article Abstract Figures Only Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Smith, C. S. Articles by Yeung, H. W. Search for Related Content PubMed PubMed Citation Articles by Smith, C. S. Articles by Yeung, H. W. Social Bookmarking                      What's this? Hotlight (NEW!) What's Hotlight?