Abstract
Objective:
To describe the ultrasound, CT findings, and clinical manifestations of pathologically confirmed skeletal muscle metastases involving trunk and pelvis.
Methods:
71 patients with 71 skeletal muscle metastases of the trunk and pelvis, pathologically proven by ultrasound-guided biopsy, were included in the study, and ultrasound findings were reviewed. CT findings were reviewed for 60 patients who underwent post-contrast CT obtained prior to biopsy, which included skeletal muscle metastases. Medical records, including the type of primary malignancy, presence of coexisting distant metastasis, and method of detection that led to referral for biopsy, were reviewed.
Results:
Most skeletal muscle metastases were hypoechoic (98.6%) with well-defined margins (85.9%), round-to-oval (47.9%), or lobulated (42.2%) with intralesional vascularity (64.8%). Typical CT findings included abscess-like lesions with rim enhancement (53.3%) or round-to-oval lesions with homogeneous enhancement (40.0%). The most common primary malignancy was lung cancer (49.3%), followed by gastrointestinal cancer (7.0%). Distant metastases other than muscle metastases were found in 84.5% of patients, and coexisting skeletal muscle metastases were found in 47.9%. CT was the most common detection method for metastases (57.8%), being more common than positron emission tomography-CT (22.5%).
Conclusion:
The current study describes the typical imaging findings of skeletal muscle metastases of the trunk and pelvis in patients with advanced cancer. CT may play an important role in the early detection of skeletal muscle metastases, and our results may aid radiologists in their diagnosis.
Advances in knowledge:
1. Skeletal muscle metastases of the trunk and pelvis demonstrate typical imaging findings on ultrasound and CT.
2. CT may aid in the early detection of skeletal muscle metastases, which are among the rarest, and our results may aid radiologists in their diagnosis.
Introduction
Skeletal muscles are among the rarest sites for distant metastases. 1 To explain the resistance of skeletal muscles to metastatic disease, several theories regarding the mechanical, metabolic, and immunological factors of skeletal muscles have been suggested. 2,3 Although an uncommon condition, more prevalent use of sensitive imaging modalities have increased reports of skeletal muscle metastases, and also prolonged survival in cancer patients achieved by advances in systemic treatment. 1,4–8
The presence of skeletal muscle metastases has been considered a marker of aggressive disease and poor prognosis. 8 The relationship between the tumor burden of skeletal muscle metastases and patient prognoses remains largely unknown. However, reports of patients with single isolated skeletal muscle metastasis have shown significantly better survival compared with those patients with multiple skeletal muscle metastases. 3 Additionally, there are several case reports on successful local treatment of isolated skeletal muscle metastases in various primary malignancies. 9–12 Thus, we believe that early detection of subclinical skeletal muscle metastases on surveillance imaging studies could be important, given the potential of improving prognosis in subsets of patients.
18-fludeoxyglucose (FDG) positron emission tomography-CT (PET-CT), which is widely used for the surveillance of cancer recurrence and distant metastasis, has proven to be a sensitive and effective tool for detecting skeletal muscle metastases. 1,4 However, post-contrast CT is generally used for routine oncologic imaging study of the chest, abdomen, and pelvis, which results in patients undergoing contrast-enhanced CT more commonly than PET-CT. 13 Unlike CT of the upper or lower extremities, detecting skeletal muscle metastases on CT of the trunk and pelvis can be challenging for radiologists as we tend to focus on detecting abnormalities within the thoracic or abdominal cavity. The common sites of skeletal muscle metastases and the corresponding CT findings of the lesions arising within chest CT, abdomen and pelvis CT, have not yet been investigated in detail. Moreover, radiologic findings of skeletal muscle metastases on ultrasound, which can be used for imaging diagnosis and guiding modality for biopsy of skeletal muscle lesions, have scarcely been reported. 14,15 We believe that investigating the radiologic findings of skeletal muscle metastases arising from the trunk and pelvis could possibly help and encourage radiologists with the detection of these lesion. In addition, reviewing the clinical manifestations of these patients would contribute to broadening the understanding of this rare group of patients.
The study aimed to describe the ultrasound and CT findings of pathologically confirmed skeletal muscle metastases involving the trunk and pelvis. We also reviewed the clinical manifestations of the lesions at the time of biopsy.
Methods and materials
Patients
This retrospective study was approved by our institutional review board, which waived the requirement for informed consent. A total of 3517 ultrasound-guided biopsies were referred to and performed at the musculoskeletal radiology department in Samsung medical center between April 2010 and September 2021. Among these patients, we identified 225 patients with malignant masses involving the skeletal muscles of the trunk and pelvis (based on a search for keywords in the reports), which were pathologically proven by assessment of tissue specimens acquired through ultrasound-guided biopsy. The following exclusion criteria were used: (a) direct invasion of the skeletal musculature via extension from tumors involving the bone, abdominal, or thoracic cavity (n = 63); (b) primary muscle sarcoma and primary or secondary muscle lymphoma (n = 82); and (c) seeding lesions at the surgical incision site (n = 10). We also searched for cases with CT-guided biopsy performed for skeletal muscle biopsy during the same period, but no such case was identified. Finally, 71 consecutive patients (46 men and 25 women; age 36–80 years; mean, 55.12 years) with 71 skeletal muscle metastases were included in the study.
Ultrasound technique and image analysis
Ultrasound-guided biopsies were performed with a single ultrasound scanner equipped with 5–1 MHz convex, 12–5 and 15–7 MHz linear transducers (iU22, Philips Medical Systems, Bothell, WA) and an 18-gauge semi-automatic core biopsy needle (Acecut; TSK Laboratory, Tochigi, Japan). Two radiologists (S.Y.C with 1 year of experience in musculoskeletal radiology and H.S.K with 6 years of experience in musculoskeletal radiology) reviewed the following ultrasound imaging features and then reached a consensus: (a) echogenicity pattern (determined based on comparison with the echogenicity of adjacent muscle; homogeneously hypoechoic, heterogeneously hypoechoic, isoechoic, heterogeneously hyperechoic, homogeneously hypoechoic, or cystic), (b) margin (well-defined, ill-defined), (c) intralesional vascularity (present, absent), (d) shape (lobulated, irregular, round-to-oval), and (e) posterior features (insignificant, posterior acoustic enhancement, posterior acoustic shadowing). The image quality of all examinations were considered acceptable.
CT technique and image analysis
For chest CT, typical imaging parameters were 0.625–0.5 mm collimation, 1.375–1.5 pitch, 2.5–3.0 mm reconstructed section, 120-kVp peak voltage, and 100–150-mAs tube current–time product. Contrast-enhanced CT images were obtained 70 s after the injection of 80–100 ml of non-ionic contrast media at a rate of 3 ml s−1 using an automatic power injector. For abdomen and pelvis CT, typical imaging parameters were 0.625–0.5 mm collimation, 0.750–0.984 pitch, 2.5–5 mm thickness of reconstructed section, 120-kVp peak voltage, and 180–240-mAs tube current–time product. Contrast-enhanced CT images were obtained at the portal venous phase with a 70 s delay after injection of 120 ml of a non-ionic contrast media at a rate of 3–4 ml s−1 using an automatic power injector.
60 patients (88.7%) had post-contrast CT obtained prior to biopsy, which included the skeletal muscle metastases. CT findings were also reviewed by a consensus of two radiologists. CT imaging features were assessed according to the classification system proposed by Surov et al as follows. 6
Type 1: round-to-oval lesions with homogeneous contrast enhancement
Type 2: abscess-like lesions with central low attenuation and rim contrast enhancement
Type 3: diffuse muscle infiltration with swelling and inhomogeneous contrast enhancement
Type 4: intramuscular calcification
Type 5: intramuscular bleeding
In addition, for patients who had multiple and post-contrast CT examinations, prior CT images were reviewed; the initial CT that showed the lesion was searched for, and the number of days between the initial CT examination and biopsy were recorded. Coexisting skeletal muscle metastasis was defined as the presence of an intramuscular lesion with imaging features similar to those of biopsy-proven muscle metastasis on CT or PET-CT.
Review of clinical data
One radiologist (S.Y.C) reviewed the medical records, including the type of primary malignancy, presence of coexisting distant metastasis, and method of detection, which led to referral for biopsy (e.g. by CT or by palpation). The radiologist also reviewed the CT radiology reports regarding whether the lesions were mentioned, and how they were interpreted.
Results
Clinical data
The clinical characteristics of 71 patients with biopsy-confirmed skeletal muscle metastases are summarized in Table 1. Among the 71 cases, CT was the most common method for detection (41, 57.8%), and radiology reports suggested the possibility of skeletal muscle metastases and led to referral for biopsy. PET-CT was the second most common method of detection (16, 22.5%), followed by physical palpation (9, 12.7%) and MRI (5, 7.0%). Among the 41 patients with CT-detected lesions, 27 had CT examinations performed prior to the CT that detected metastases. Among them, 20 showed evident skeletal muscle metastases on CT, but were not mentioned in the radiology report at the time. Along with the 41 CT-detected cases, retrospective analyses revealed 19 additional patients who were found to have CT scans taken before biopsy, which demonstrated skeletal muscle metastasis. However, they were not mentioned in the radiology report. These 19 patients were referred for biopsy after detection on PET-CT.
Table 1.
Clinical characteristics of 71 biopsy-confirmed skeletal muscle metastases
| Clinical characteristics | Skeletal muscle metastases (n = 71) |
|---|---|
| Method of detection | |
| CT | 41 (57.8%) |
| PET-CT | 16 (22.5%) |
| Palpation | 9 (12.7%) |
| MRI | 5 (7.0%) |
| Primary malignancy | |
| Lung cancer | 35 (49.3%) |
| Gastrointestinal tumor | 5 (7.0%) |
| Gynecologic tumor, sarcoma | 4 (5.6%) each |
| Breast cancer, multiple myeloma, carcinoma of unknown primary | 3 (4.2%) each |
| Hepatocellular carcinoma, renal cell carcinoma, thyroid cancer, melanoma, head and neck tumor | 2 (2.8%) each |
| Pancreatic cancer, malignant mesothelioma, peritoneal cancer, skin cancer | 1 (1.4%) each |
| Other distant metastasis | |
| Present | 60 (84.5%) |
| Absent | 11 (15.5%) |
| Coexisting muscle metastasis | |
| Present | 34 (47.9%) |
| Absent | 37 (52.0%) |
PET, positron emission tomography.
The most common sites of skeletal muscle metastases in the trunk and pelvis were the thorax (40.9%), abdominal wall (23.9%), paraspinal region (19.7%), and buttock (15.5%) (Figure 1). Involved muscles for each anatomical regions were as follows: (1) thorax: trapezius, latissimus dorsi, intercostal, serratus anterior, rhomboid, pectoralis major, infraspinatus, teres major; (2) abdominal wall: rectus abdominis, oblique muscle; (3) paraspinal: longissimus, semispinalis, multifidus, iliocostalis lumborum; and (4) buttock: gluteus maximus, medius, minimus. The most common primary malignancy was lung cancer (35/71, 49.3%), followed by gastrointestinal tumor (5/71, 7.0%). Distant metastases other than skeletal muscle metastases were found in 84.5% (60/71) of patients. Coexisting skeletal muscle metastases were found in 47.9% (34/71) of patients. Six patients had a single isolated skeletal muscle metastasis with no other metastases anywhere else.
Figure 1.
Sites of skeletal muscle metastases in trunk and pelvis. Involved sites and muscles of a total of 71 biopsy-confirmed skeletal muscle metastases are depicted.
Imaging findings of skeletal muscle metastasis
The results of the ultrasound imaging analyses of skeletal muscle metastasis are summarized in Table 2. Regarding echogenicity, most skeletal muscle metastases were either heterogeneously hypoechoic (38/71, 53.5%) or homogeneously hypoechoic (32/71, 45.1%) in nature (Figures 2–8). Most lesions showed well-defined margins (85.9%). Shapes of the lesions were most commonly round-to-oval (34/71, 47.9%), followed by lobulated (30/71, 42.2%) and irregular shapes (7/71, 9.9%). Intralesional vascularity was demonstrated in 64.8% of cases, and the insignificant posterior acoustic features were found in 70.4%. The mean size was 4.1 cm, ranging from 1.1 to 16 cm.
Table 2.
Ultrasound findings of 71 biopsy-confirmed skeletal muscle metastases
| Clinical characteristics | Skeletal muscle metastases (n = 71) |
|---|---|
| Echogenicity | |
| Heterogeneously hypoechoic | 38 (53.5%) |
| Homogeneously hypoechoic | 32 (45.1%) |
| Heterogeneously hyperechoic | 1 (1.4%) |
| Margin | |
| Well-defined | 61 (85.9%) |
| Ill-defined | 10 (14.1%) |
| Shape | |
| Round-to-oval | 34 (47.9%) |
| Lobulated | 30 (42.2%) |
| Irregular | 7 (9.9%) |
| Intralesional vascularity | |
| Present | 46 (64.8%) |
| Absent | 25 (35.2%) |
| Posterior acoustic features | |
| Insignificant | 50 (70.4%) |
| Posterior acoustic enhancement | 19 (26.8%) |
| Posterior acoustic shadowing | 2 (2.8%) |
| Size (cm) | |
| Mean (range) | 4.1 (1.1–16) |
Figure 2.
A 43-year-old male patient with history of alveolar soft part sarcoma involving the right thigh. Grayscale ultrasound image (a) obtained during biopsy shows a 2.1 cm well-circumscribed heterogeneously hypoechoic oval-shaped mass involving the left external oblique muscle. Power Doppler ultrasound image (b) demonstrates intralesional vascular flow. Post-contrast axial abdomen and pelvis CT image (c) shows an oval lesion (arrow) with homogenous enhancement (Type 1) that corresponds to the mass depicted on ultrasound. The patient also had multiple liver metastases (d).
Figure 3.
A 73-year-old male patient with history of lung cancer. Power Doppler ultrasound image (a) obtained during biopsy shows a 3.8 cm well-circumscribed heterogeneously hypoechoic oval-shaped mass with intralesional vascular flow involving the left infraspinatus muscle. Post-contrast axial (b) and coronal (c) chest CT images show abscess-like lesion (arrow) with central low attenuation and rim enhancement (Type 2) which corresponds to the mass depicted on ultrasound. The patient also had multiple bone and distant lymph node metastases (not shown).
Figure 4.
An 85-year-old male patient who had lung cancer with lung-to-lung metastases. Grayscale ultrasound image (a) obtained during biopsy shows a 3.0 cm ill-defined heterogeneously hypoechoic lobulated mass involving the right paraspinal muscle. Post-contrast axial chest CT image (b) shows an abscess-like lesion (arrow) with central low attenuation and rim enhancement (Type 2) that corresponds to the mass depicted on ultrasound. Post-contrast coronal CT image demonstrates (c) another metastasis (arrowhead) in the contralateral paraspinal muscle as a rim enhancing lesion.
Figure 5.
A 45-year-old male patient with history of renal cell carcinoma. Grayscale ultrasound image (a) obtained during biopsy shows a 3.0 cm well-circumscribed heterogeneously hypoechoic oval-shaped mass involving the left latissimus dorsi. Post-contrast axial chest CT image (b) shows two abscess-like lesions (arrows) with central low attenuation and rim enhancement (Type 2) involving the left latissimus dorsi. Post-contrast axial chest CT image acquired 3 months prior (c) revealed smaller identifiable lesions with homogeneous contrast enhancement (Type 1, arrowheads).
Figure 6.
A 50-year-old female patient with history of lung cancer. Grayscale ultrasound image (a) obtained during biopsy shows a 1.1 cm well-circumscribed hypoechoic oval-shaped mass involving the left rectus abdominis muscle. Color Doppler ultrasound image (b) does not demonstrate intralesional vascular flow. Post-contrast axial abdomen and pelvis CT image (c) shows an oval lesion (arrow) with homogenous enhancement (Type 1) that corresponds to the mass depicted on ultrasound. Axial fat-suppressed 3D volumetric interpolated breath-hold examination T 1 weighted image with contrast administration (d) shows an oval lesion (arrow) with homogenous enhancement.
Figure 7.
A 66-year-old male patient with history of lung cancer. Grayscale ultrasound image (a) obtained during biopsy shows a 4.1 cm well-circumscribed heterogeneously hypoechoic oval-shaped mass involving the right gluteus medius muscle. Color Doppler ultrasound image (b) demonstrates vascular flow at the periphery of the lesion. Post-contrast axial abdomen and pelvis CT image (c) shows abscess-like lesion (arrow) with central low attenuation and rim enhancement (Type 2) that corresponds to the mass depicted on ultrasound.
Figure 8.
A 46-year-old female patient with history of dermatofibrosarcoma protuberans of left thigh. Grayscale ultrasound image (a) obtained during biopsy shows a 3.5 cm well-circumscribed heterogeneously hypoechoic round-shaped mass involving the left longissimus muscle. Color Doppler ultrasound image (b) demonstrates intralesional vascular flow. Post-contrast axial abdomen and pelvis CT image (c) shows abscess-like lesion (arrow) with central low attenuation and rim enhancement (Type 2) that corresponds to the mass depicted on ultrasound. Axial T 2 weighted image (d) of the lumbar spine MRI shows hyperintense mass (arrow).
The results of CT imaging analyses are summarized in Table 3. Skeletal muscle metastases tended to present as abscess-like lesions with central low attenuation and rim enhancement (Type 2; 32/60, 53.3%, Figures 3–5) or as round-to-oval lesions with homogeneous enhancement (Type 1; 24/60, 40.0%, Figure 2). Four cases of metastases were demonstrated as diffuse muscle infiltration with swelling and inhomogeneous contrast enhancement (Type 3), whereas no case of intramuscular calcification or hemorrhage was observed.
Table 3.
CT findings of 60 biopsy-confirmed skeletal muscle metastases
| CT findings | Skeletal muscle metastases (n = 60) |
|---|---|
| Type 1 | 24 (40.0%) |
| Type 2 | 32 (53.3%) |
| Type 3 | 4 (6.7%) |
| Type 4 | 0 |
| Type 5 | 0 |
Type 1: round-to-oval lesions with homogeneous contrast enhancement; Type 2: abscess-like lesion with central low attenuation and rim contrast enhancement; Type 3: diffuse muscle infiltration with swelling and inhomogeneous contrast enhancement; Type 4: intramuscular calcification; and Type 5: intramuscular bleeding.
Discussion
In this study, we reviewed the ultrasound findings of 71 metastases and CT findings of 60 metastases involving skeletal muscles of the trunk and pelvis, which were pathologically confirmed through ultrasound-guided biopsies. The most common presentation on ultrasound was a well-defined hypoechoic lesion with a round-to-oval or lobulated shape and intralesional vascularity. The majority of skeletal muscle metastases were demonstrated as abscess-like lesions with central low attenuation and rim enhancement or as round-to-oval lesions with homogeneous enhancement on CT. The involved muscles included the thorax, abdominal wall, paraspinal region, and buttock muscles.
A review of the clinical data of 71 cases revealed CT to be the most common method for the detection of metastases (41, 57.8%), which was more common than by PET-CT (16, 22.5%). Although CT was the most common method for the detection of trunk and pelvis skeletal muscle metastases in our study, a retrospective review revealed an additional 19 patients who were found to have skeletal muscle metastases on CT, which were not mentioned in the radiology report. In addition, among 41 skeletal muscle metastases that were referred for biopsy after detection on CT, retrospective analyses of prior CT scans showed that 20 of them were evident on the image, but not mentioned in the radiology report at the time. These results suggest that the incidence of skeletal muscle metastases might be underestimated as they could easily remain undetected on CT. Although it is a challenging task, radiologists may serve a substantial role in the early diagnosis of skeletal muscle metastases by detecting them on chest, abdomen and pelvis CT.
Lung cancer was the most common primary malignancy (35, 49.3%), comprising nearly half of the cases, which is consistent with the results of previous studies. 1,16–19 Other studies reported genital, 6 gastrointestinal, 20 and breast cancers 21 to be most common primary malignancies, in their series. This inconsistency may be related to differences in patient cohorts with varying numbers. The presence of other distant metastases comprised the majority of cases (60, 84.5%), whereas isolated skeletal muscle metastases were less common (11, 15.5%). Previous studies have suggested that locoregional treatment could be applied to improve prognosis in cases of isolated skeletal metastases. 9–12 Thus, the early detection of skeletal muscle metastases could be especially important in this subset of patients. Our results showed that isolated skeletal muscle metastases constitute a relatively small portion, but it may be worthwhile to identify these patients at an earlier stage.
We classified CT manifestations of skeletal muscle metastases according to the classification system proposed by Surov et al. 6 Several studies have reported CT findings of skeletal muscle metastases according to this classification system. 16,20,21 Although there was inconsistency in the reported results among the studies, round-to-oval lesions with homogeneous enhancement (Type 1) or abscess-like lesions with central low attenuation and rim enhancement (Type 2) were observed in the majority of cases, which is in general agreement with our study results. Unlike in previous reports, there were no cases of metastasis that presented as calcification or hemorrhage. These findings may not be specific or conspicuous, especially when they are small. However, it may be important for radiologists to inspect skeletal muscles for the possible presence of these lesions when evaluating the chest, abdomen and pelvis CT scans of patients with a history of malignancy.
Ultrasound findings of skeletal muscle metastases have scarcely been reported. 14,15 Our study revealed that the most common presentation of skeletal muscle metastases on ultrasound was a well-defined hypoechoic lesion with a round-to-oval or lobulated shape and intralesional vascularity. These findings are relatively non-specific and overlap with numerous benign and malignant conditions. 22–24 However, it may be worthwhile to report these findings, as prior knowledge of these findings may aid in ultrasound localization of the lesion detected on CT prior to performing biopsy. In addition, one may encounter a patient with a history of malignancy who is referred for primary evaluation of an intramuscular mass with ultrasound. In such a situation, prior knowledge of ultrasound findings of skeletal muscle metastases may aid in deciding whether to perform a biopsy of the lesion.
In addition to the intrinsic limitations of this retrospective study, we acknowledge some limitations. First, the radiological findings of skeletal muscle metastases were not statistically compared with those of benign intramuscular lesions. Second, the CT and ultrasound findings were relatively non-specific, and quantitative imaging parameters were not sought. Third, although our study included one of the largest samples of pathologically proven skeletal muscle metastases to our knowledge, the number of cases is still limited. In addition, selection bias may have been introduced by including only pathologically confirmed lesions. We thought it was necessary that several intramuscular lesions, including primary soft tissue tumors, abscesses, or sarcoidosis, could mimic the radiological findings of skeletal muscle metastasis. 25 However, we cannot deny the possible effect of our inclusion criteria on the results differing from the results of previous studies those determined patient group based on image analyses, such as relatively high percentage of isolated skeletal muscle metastases or difference in major imaging modalities for detecting metastases. 6,26 Fourth, only one author reviewed the medical record. Finally, the role of early detection of skeletal muscle metastases in the prognosis of patients remains unclear. Further studies are warranted to elucidate its significance.
In conclusion, we described the ultrasound and CT findings and clinical manifestations of skeletal muscle metastases involving the trunk and pelvis, which were pathologically confirmed. We also reviewed clinical data regarding the clinical presentation at the time of biopsy. The most common presentation on ultrasound was a well-defined hypoechoic lesion, round-to-oval or lobulated shape and intralesional vascularity. The majority of skeletal muscle metastases were demonstrated as abscess-like lesions with central low attenuation and rim enhancement or as round-to-oval lesions with homogeneous enhancement on CT. The involved muscles included the thorax, abdominal wall, paraspinal region, and buttock muscles. The most common method for the detection of metastases was CT. Although it may be challenging for radiologists to detect skeletal muscle metastases on CT, they can serve a substantial role in the early detection of these lesions. Our results may aid in the detection of skeletal muscle metastases and broaden the understanding of this rare group of diseases. Further studies on the role of early detection of skeletal muscle metastases in prognoses are warranted.
Contributor Information
So Yeon Cha, Email: sy0501.cha@gmail.com.
Hyun Su Kim, Email: calmuri@naver.com.
Ji Hyun Lee, Email: carrot302@hotmail.com.
Young Cheol Yoon, Email: youngcheol.yoon@gmail.com.
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