PET/CT imaging of skeletal muscle metastases

Introduction

Although the skeletal musculature represents approximately 50% of the body mass, skeletal muscle metastases (SMM) are very rare because of complex resistance of the musculature to metastatic invasion (1–3). The prevalence of SMM in autopsy varies from 0.03% to 5.6% (4,5). Radiological studies reported a prevalence of muscle metastases from 1.2% to 1.8% (6,7).

According to the literature, SMM present with several radiological features (6–9). For example, on computer tomography (CT) five different patterns of SMM were described: intramuscular mass (type I), abscess-like intramuscular lesion (type II), diffuse metastatic muscle infiltration (type III), multiple muscle calcifications (type IV), and intramuscular bleeding (type V) (7). On MRI, most reported features of SMM were solitary or multiple intramuscular lesions with hyperintense signal in comparison to unaffected musculature on T2-weighted images and isointense signal on T1-weighted images with marked enhancement (8,9).

In the past, predominantly isolated case reports dealt with unusual incidental findings in positron emission tomography (PET) imaging of SMM (10–12). It is unknown, if SMM features in PET/CT are different in several primary malignancies.

Therefore, the aim of this study was to analyze PET/CT findings of SMM in a larger group of patients and to determine PET patterns of SMM in different primary tumors.

Material and Methods

Institutional data acquisition

Between January 2009 and December 2011 581 patients with lung cancer were investigated by positron emission tomography with 18 F-fluordeoxyglucose (FDG PET) and computed tomography (CT) at the Center of Fusion Imaging, Halle.

In all cases, whole body PET/CT was performed on an integrated scanner (Siemens 16 Biograph, Siemens, Erlangen, Germany). PET images were obtained in three dimensional mode for 3 min per bed position after intravenous application of 5 MBq of FDG per kg of body weight.

CT scans were performed prior to PET. Typical imaging parameters were 120 kVp, 85 mAs, and 3 mm slice thickness. The acquired images were interpreted retrospectively by two radiologists (AS and MP with 9 and 12 years of experience, respectively).

We reviewed the electronic database for muscle involvement in malignant diseases (analysis of the reports). In 39 cases abnormal activity in skeletal muscles had been described. After reviewing the images of these 39 patients, in 28 cases subcutaneous or osseous metastases with secondary invasion of adjacent musculature were found. In six patients the described abnormal muscle uptake was judged as still physiological. In the remaining five patients skeletal muscle metastases (SMM) were positively identified. All patients were men with a median age of 62 years, ranging from 42 to 67 years (Table 1). The diagnosis of SMM had been confirmed histopathologically in two cases and in the other three patients it was taken on the basis of disease sequelae.

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Table 1.

Patients with SMM identified in our institution.

Patients	Age (years)	Sex	Diagnosis	Size (cm)	SUV	Muscles
1	66	M	Lung cancer	n.v.	5.1	Deltoid
				n.v.	8.0	Gluteus maximus
2	57	M	Lung cancer	n.v.	4.8	Erector spinae
3	42	M	Lung cancer	5.0	9.5	Adductor longus
4	67	M	Lung cancer	n.v.	7.4	Erector spinae
5	62	M	Lung cancer	6.5	9.8	Gluteus medius
				3.2	8.5	Gluteus medius
				1.2	5.3	Gluteus minimus
				1.1	6.4	Biceps femoris
				2.0	7.4	Biceps femoris

n.v., not visible on CT (investigation without intravenous application of contrast medium).

Results

At our center the prevalence of SMM in lung cancer was 0.9% (five cases out of 581 patients with PET investigations). In addition, in these five patients 10 intramuscular metastases were detected (Table 1).

Furthermore, our literature search identified 33 patients with 57 SMM. Most reported metastases arise from lung cancer, esophageal cancer, and renal cell carcinoma. Other tumors were rare.

Therefore, our analysis comprised 38 patients with 67 muscle metastases. SMM were identified incidentally on staging PET/CT in 31 of the 38 patients (81.6%).

In four patients (10.5%) SMM presented as focal pain with or without swelling of the overlying skin. Clinical signs were not reported in three cases.

All identified SMM presented as focally abnormal intramuscular uptake (Figs. 1–3) with SUV ranging from 2.4 to 25.9, median SUV 7.8 (mean SUV = 9.0 ± 5.1). The median size of the muscle metastases was 2.5 cm (range, 0.6–6.5 cm; mean size, 2.7 ± 1.3 cm). OPEN IN VIEWER

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Fig. 2.

Same patient as in Fig. 1. Intramuscular metastases (arrows) in both biceps femoris muscles. (a) PET images of SMM; (b) CT scan detecting two lesions with rim enhancement and central low attenuation (arrows); (c) fusion image.

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Fig. 3.

SMM (arrow) in the deltoid muscle. (a) Focal uptake in the left deltoid muscle on PET images. Additionally a focus of uptake in the right neck resulting from a muscle activity is seen; (b) CT scan without iodinated contrast showing no abnormalities; (c) fusion images.

Most patients (n = 23, 60.5%) underwent PET/CT without additional application of iodinated contrast medium. In all of these cases, SMM were detected in PET only, and non-contrast CT scans showed no abnormality. In seven patients, CT scans were performed with contrast medium, and in four of these intramuscular metastases were also identified by PET only. In eight cases no information regarding CT scans was given.

In nine (23.7%) of the 38 patients the identified SMM were isolated distant metastases or isolated tumor recurrence.

Localization of metastases had been reported in 54 cases. SMM were localized most frequently in the trunk musculature (37%) and gluteal muscles (28%).

In most patients, esophageal cancer, lung cancer, and renal cell carcinoma were diagnosed (Table 2). There was no correlation between SUV and size of SMM (r = 0.101, P = 0.558). Furthermore, there were no significant differences between SUV of the identified SMM in esophageal cancer, renal cell carcinoma and lung cancer (Table 2). SMM from other tumors were rare and could not be included into the statistical analysis.

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Table 2.

Comparison of size and SUV of SMM from several malignancies

Esophageal cancer	RCC	Lung cancer	P values
Patients/SMM	8/19	6/7	18/34
Size, M ± SD	2.9 ± 0.9	2.1 ± 1.2	2.9 ± 1.8	0.404
SUV, M ± SD	8.4 ± 4.0	13.1 ± 9.4	8.7 ± 4.5	0.094

Discussion

There are few studies addressing SMM because of their rare occurrence (6–9,20). Whereas CT and MRI images of intramuscular metastases had been studied in large groups of patients (6–9), PET and PET/CT findings of SMM have predominantly been described as case reports (10–33). Only two studies regarding PET and PET/CT imaging of SMM have been published previously (20,34).

In addition, not every publication provided information regarding SUV of SMM. Therefore, the present study is the first report regarding PET/CT of SMM to date in a larger group of patients including SUV. Previously, one review of the literature regarding intramuscular metastases on FDG PET/CT has been reported (35). However, the authors performed no comparison of PET findings of SMM arising from several malignancies.

According to previous reports, the frequency of radiologically detected SMM ranges from 1.2% to 1.8% (6,7). There have been only few studies providing the frequency of muscle metastases in PET/CT. It has been reported as 1.6% in non-small cell lung carcinoma (20) and 1.7% in esophageal cancer (14). However, in the study of Nakatani et al., who examined patients with renal cell carcinoma by PET/CT the frequency of SMM was estimated to be 13% (three cases with SMM out of 23 patients) (13). However, the authors did not discuss this finding. The high prevalence of SMM in this study might be related to the small number of patients. Khandelwal et al. analyzed 8492 oncologic patients in their study and found SMM in 73 cases (0.86%) (34). In the present analysis, the frequency of SMM in lung cancer was 0.9% (five cases out of 581 patients).

According to the literature, most SMM are clinically asymptomatic (7). They occur often in patients with multiple metastases and have no influence on treatment of primary disease. However, SMM can be isolated distant metastases also (7). In our analysis, for example, in 23.7% of the patients the identified SMM were isolated distant metastases or isolated tumor recurrence. Therefore, it is very important to diagnose occult SMM as it may change management of the disease.

CT is the most frequent staging investigation in oncology. However, as has been mentioned previously, some SMM, especially small lesions can be underdiagnosed on CT (24,27,30,31,34–37).

In the present study, most patients who underwent PET/CT did not receive iodinated contrast medium. Therefore, a comparison between PET and CT regarding performance for detection of SMM cannot be given from our data. However, some reports suggested that PET can detect intramuscular metastases which are invisible in CT with contrast medium (20,24,27,30,31,35–37). In fact, in our analysis, four CTs with intravenous application of contrast medium were reported to show no metastatic lesions, PET/CT, however, diagnosed SMM as isolated distant metastasis (20,24,27,35). This finding suggests that PET/CT may be superior to CT alone in the diagnosis of SMM.

Our analysis shows that SMM manifest on PET/CT as focal hypermetabolic intramuscular areas with very different SUV. We found that there were no significant differences between SUV or size of the identified SMM in esophageal cancer, renal cell carcinoma, and lung cancer.

In our data, most intramuscular metastases were localized in trunk muscles and in the gluteal musculature. The finding corresponds well with those of other authors (6,7).

Our analysis has several limitations. First, this is a retrospective study and most lesions were acquired from the literature. Second, we could compare SMM from three primary malignancies only. Clearly, more data would be necessary to estimate the true prevalence of SMM in several tumors and to compare their features on PET/CT.

In conclusion, SMM manifested on PET/CT as focal hypermetabolic intramuscular areas with different SUV. There were no significant differences between SUV or size of the identified SMM in esophageal cancer, renal cell carcinoma, and lung cancer.

PET/CT may be superior in the detection of SMM in comparison to CT.