MRI features of different types of sinonasan rhabdomyosarcomas: a series of eleven cases

Abstract

Objective:

To retrospectively analyze magnetic resonance imaging (MRI) features of various pathological subtypes of sinonasal rhabdomyosarcoma (RMS) and explore correlations between imaging features and pathological subtypes.

Methods:

In total, 11 cases with embryonal, alveolar or pleomorphic sinonasal RMSs, confirmed by surgical pathology, were selected. Their characteristics and distinctive imaging features were analysed, and the correlation between pathology and imaging features was explored.

Results:

Bone destruction was observed in all 11 cases with RMS. Expansive growth was predominant in three alveolar and three embryonal RMS cases, and creeping growth was predominant in two alveolar, two embryonal and one pleomorphic RMS cases. Signs of residual mucosa were observed in all 11 cases, and 10 cases showed involvement of multiple sinus cavities and orbital cavities. All cases exhibited mild-to-intermediate enhancement.

Conclusion:

Sinonasal RMSs have the following characteristic MRI features: ethmoid sinuses and middle nasal conchae are the prevalent sites; lesions are mainly of mild enhancement; tumours exhibit signs of residual mucosa, mild-to-intermediate enhancement and frequent orbital involvement; bone invasion and bone destruction are frequently observed; and haematogenous metastasis is not as common as lymphatic metastasis. RMSs of various pathological subtypes were not significantly distinct by imaging.

Introduction

Rhabdomyosarcomas (RMSs) are malignant tumours originating from striated muscle tissues or mesenchymal tissues differentiating into striated muscles. Most RMS cases are observed in children, in whom RMSs account for 4–8% of paediatric malignant tumours, mainly in the urinary system, head and neck, limbs and retroperitoneum; however, RMSs are rarely observed in adults.¹ Since there is no striated muscle tissue in the sinonasal area, sinonasal RMS cases are very rare and prone to misdiagnosis. To the authors’ knowledge, approximately 340 cases of sinonasal RMS have been documented to date; however, they mainly focused on the investigation of pathological and clinical characteristics (such as treatment efficacy, overall survival and potential prognostic factors), with few studies analyzing the imaging features of sinonasal RMS.^2–5 Of note, a recent multiparametric MRI study showed apparent diffusion coefficients (ADCs) of sinonasal RMS decreased significantly in comparison with sinonasal carcinomas, suggesting ADCs may be an important tool for differentiating sinonasal RMS from sinonasal cancers.⁶ However, this study is advanced MRI techniques (such as diffusion-weighted imaging and dynamic contrast-enhanced examination) dependent, with imaging findings on conventional MRI insufficiently investigated.

Correct preoperative diagnosis of sinonasal RMS is crucial for otolaryngologists to avoid unnecessary extensive surgery as well as inappropriate option of non-surgical treatments (such as chemotherapy/radiotherapy). Nevertheless, owing to the non-specific clinical features and inadequate knowledge of radiological findings, it is easy to misdiagnose sinonasal RMS as other malignant tumours in sinonasal area. In addition, it is documented that RMSs could be subdivided into different subtypes with the most common being embryonal (ERMS) and alveolar (ARMS).² Furthermore, various pathological subtypes of RMS result in differential prognoses. For example, a number of previous studies reported that ARMS has a significantly worse prognosis in comparison to the other subtypes.^2,5,7,8 Therefore, detailed investigation to the MRI features of different subtypes of sinonasal RMS is of great importance for clinicians to perform personalized treatments.

The aim of this study was to improve the likelihood of performing accurate preoperative diagnosis and to provide further information on the treatment outcomes and postoperative follow-up strategy of this rare malignancy.

Methods and materials

Patients

Details of 11 patients with sinonasal RMSs treated in Xiangya hospital, Central South University (n = 9) and Heyuan People’s Hospital (n = 2) from January 2003 to December 2019 were retrieved from the database. All cases of sinonasal RMSs were confirmed by histopathological examination. All the eleven patients had complete MRI images and were included in the study. This retrospective study was approved by the institutional review board of our hospital, and the requirement for informed consent was waived.

Examinations

Routine MRI scans and contrast-enhanced (CE) examinations were performed in all enrolled patients prior to each surgery. The patients underwent MR imaging on a 1.5 T MR scanner (Signa Hdxt General Electrics, Milwaukee, USA) and 3.0 T MR Scanner (Signa Hdxt General Electrics, Milwaukee, USA), with an 8-channel head/neck coil. Routine axial scans were performed with spin-echo-T1W imaging (T1WI) and fast spin-echo-T2W imaging (T2WI) sequences. CE-T1WI was used for enhancement, with a slice thickness of 5 mm, slice space of 5 mm and field of view of 195 × 240. Axial and coronal images were obtained during non-CE scans, while axial, coronal and sagittal images were obtained during CE-scans, with fat suppression. The imaging parameters were as follows: T1WI: echo time (TE) = 10 ms, repetition time (TR) = 400 ms; T2WI: TE = 98 ms, TR = 4,200 ms, 354 × 512 matrix and gadolinium-diethylenetriaminepentaacetic acid as the contrast agent at 0.2–0.3 mmol/kg.

Image analysis

Two experienced head and neck radiologists, with over 20 years of experience in imaging of the head and neck reviewed all images retrospectively. To avoid the potential bias induced by observers’ individual decisions/scorings in the process of imaging assessment, we used the κ coefficient to evaluate the degree of agreement between obtained and predicted values. The ranking order of k value is from 0 to 1, where 0 means that there is no agreement, and one means complete agreement.⁹ The range 0.8–1.0 is considered excellent agreement, 0.6–0.8 good agreement, 0.4–0.6 moderate agreement, 0.2–0.4 fair agreement, and less than 0.2 poor agreements.⁹ In the present study, the radiologists/otolaryngologists first received a prior professional training to obtain a uniform recognition to the fundamental imaging signs such as the signal intensity, enhancement pattern and bone invasion. Second, the observers assessed the lesions’ imaging features independently. Finally, the assessment results provided by the observers were obtained to calculate the k value using K statistics (Supplementary table 1).

The image assessment includes the centre of the lesion (site of origin), the involvement of multiple sinus cavities and the adjacent structures (bone, orbit, intracranial), lymph node metastasis, residual mucosa and lesion morphology, signal intensity and enhancement degree. The definition of degree of enhancement: compared with that in the muscle, the degree of enhancement was defined as mild, moderate (between the muscle and mucosa) or significant (equivalent to that in the mucosa). Signs of residual mucosa: refers to the residual presence of the mucosa at the lesion. Sites with a complete absence of the mucosa were considered to be the centres of lesions. The tumour extended along the submucosa, and the residual mucosa was clearly observable at the periphery as intense signals on T2WI of MRI and significant homogeneous linear enhancement; the features were consistent with those of the normal mucosa.

Results

Eleven cases with presurgical MRI examinations were enrolled in this study, and the MRI features were summarized. There were five females (45%) and six males (55%) patients, with an age range of 7–40 years, median age 29 years and average age 28 years. Nine (72%) patients were between 20 and 40 years old, and two patients were younger than 18 years. The reported symptoms included nasal obstruction, epistaxis, headache, exophthalmos and strabismus. There were five alveolar (45.5%), five embryonal (45.5%) and one pleomorphic (9%) cases.

All 11 cases exhibited mixed hypointense signals on T1WI, mixed hyperintense signals on T2WI (compared with the cerebral cortex) and mild enhancement on CE-T1WI. The RMSs originated (centre of the tumour) from the maxillary sinus in one case, ethmoid sinuses and middle nasal conchae in six cases, ethmoid sinuses and the superior nasal concha in one case, ethmoid sinuses in one case, ethmoid and frontal sinuses in one case and the nasopharynx and ethmoid sinuses in one case. There were four alveolar and two embryonal cases with expansive growth pattern, two alveolar and two embryonal cases with creeping growth pattern and one pleomorphic case with creeping growth pattern, along with mild expansive features. Bone destruction was observed in all 11 cases, with 10 cases showing orbital invasion and one case showing orbital and intracranial invasions. The clinical features and imaging features are summarized in Tables 1 and 2.

Table 1.

Clinical features of 11 cases with rhabdomyosarcoma

Case	Sex/Age (years)	RMS subtype	Centre of RMS	Multisinus involvement	Orbital invasion	Cranial invasion	Cervical lymph node metastases
1	F/12	Alveolar	Right maxillary sinus	Right maxillary sinus, ethmoid sinuses, middle nasal concha	Y	N	N
2	F/32	Alveolar	Right ethmoid sinus, middle nasal concha	Bilateral ethmoid sinuses, right middle nasal concha, inferior nasal concha	Y	N	Right submandibular region
3	F/40	Alveolar	Left ethmoid sinus, middle nasal concha	Left ethmoid sinus, middle nasal concha, maxillary sinuses, sphenoid sinuses	Y	N	Left parapharyngeal space
4	M/27	Alveolar	Left ethmoid sinus, superior nasal concha	Bilateral ethmoid sinuses, frontal sinuses, left middle nasal concha, inferior nasal concha	Y	Y	Left submandibular region
5	M/20	Alveolar	Right ethmoid sinus, middle nasal concha	Right middle nasal concha, inferior nasal concha, ethmoid sinuses, choanae, nasopharynx, maxillary sinuses	Y	N	Bilateral parapharyngeal space, right cervical region
6	M/39	Pleomorphic	Right ethmoid sinus, frontal sinuses	Bilateral frontal sinuses, ethmoid sinuses, right middle nasal concha	Y	N	N
7	F/36	Embryonal	Left ethmoid sinus, middle nasal concha	Left ethmoid sinus, maxillary sinuses, middle nasal concha	Y	N	N
8	F/29	Embryonal	Right ethmoid sinus	Right ethmoid sinus, frontal sinuses, maxillary sinuses, inferior and middle nasal conchae	Y	Mild	Right submandibular region
9	M/39	Embryonal	Left ethmoid sinus, middle nasal concha	Bilateral ethmoid sinuses, frontal sinuses, middle nasal concha, left inferior nasal concha, left maxillary sinus, bilateral nasopharynxes	Y	Y	Bilateral parapharyngeal space, cervical region, submandibular region
10	M/7	Embryonal	Choanae, nasopharynxes	Choanae, nasopharynxes	N	N	N
11	M/29	Embryonal	Right middle nasal concha, ethmoid sinuses	Right middle nasal concha, ethmoid sinuses, maxillary sinuses, inferior nasal concha, frontal sinuses	Y	N	N

N, No;Y, Yes.

Table 2.

Imaging features of 11 cases of rhabdomyosarcoma

Case	RMS subtype	T1WI	T2WI	CE-T1WI	Residual mucosa	Growth pattern	Bone destruction
1	Alveolar	Hypointense, heterogeneous	Hyperintense, heterogeneous	mild	marginal	Mainly expansive	Y
2	Alveolar	Hypointense, heterogeneous	Hyperintense, heterogeneous	moderate	marginal	Mainly expansive	Y
3	Alveolar	Hypointense	Hyperintense, heterogeneous	mild	central	Mainly creeping	Y
4	Alveolar	Hypointense, heterogeneous	Hyperintense, heterogeneous	mild	marginal	Mainly expansive	Y
5	Alveolar	Hypointense	Hyperintense	mild	marginal	Mainly creeping	Y
6	Pleomorphic	Hypointense, heterogeneous	Hyperintense, heterogeneous	mild	central	Mainly expansive	Y
7	Embryonal	Hypointense, heterogeneous	Hyperintense, heterogeneous	mild	central	Mainly expansive	Y
8	Embryonal	Hypointense, heterogeneous	Hyperintense, heterogeneous	mild	central	Mainly creeping	Y
9	Embryonal	Hypointense, heterogeneous	Hyperintense, heterogeneous	mild	central	Mainly creeping	Y
10	Embryonal	Hypointense, heterogeneous	Hyperintense, heterogeneous	mild	marginal	Mainly expansive	Y
11	Embryonal	Hypointense, heterogeneous	Hyperintense, heterogeneous	moderate	marginal	Mainly expansive	Y

N, No;Y, Yes.

Discussion

RMSs are highly malignant soft tissue tumours originating from the mesoderm. The incidence of RMS of organs without striated muscles is much higher than that of organs with striated muscles. Misdiagnosis is common with non-striated muscle organ RMS, which originates from multipotent primitive mesenchymal tissues cells or metaplasia of early ectopic striated myoblasts to abnormal sites with malformations.¹⁰ Previous studies have suggested that RMS mostly occurs in children under 18 years of age.^11,12 By contrast, 70% of our cases were adults, and there was no significant difference in the incidence rate between males and females.

RMS has four subtypes, namely, alveolar, embryonal, botryoid and pleomorphic. The prognosis of RMS is mainly correlated with the pathological stage, and the effects of histological types on the prognosis are divergent. Alveolar tumours are usually more aggressive than embryonal tumours, and mixed tumours generally behave as alveolar tumours.¹³ Currently, MRI is the best method for preoperative staging of RMS. However, the use of MRI to distinguish pathological subtypes of RMS has rarely been reported.

The sinonasal walls consist of the mucosa, muscularis mucosa and bony wall. The muscularis mucosa differentiates from multipotent mesenchymal tissue, and RMS may arise from certain mutations during the differentiation process. All 11 cases in this study showed signs of a residual mucosa, central or marginal to the lesion (Figures 1–3), indicating that the tumour grew and extended along the submucosa and displaced the mucosa, while the mucosa at the centre of the lesion was destructed and replaced by tumour tissue. Sinus RMSs have been reported to only squeeze the mucosa,¹⁴ which is highly consistent with the findings of this study. The residual mucosa exhibited hypointense signals on T2WI (occasionally highly hypointense signals), hyperintense signals on T1WI and marked enhancement; these features were consistent with those of the normal mucosa. The hyperintense signals on T1WI and hypointense signals on T2WI were probably due to a residual mucus stemming from blockage of mucous glands caused by oversqueezing of the mucosa (Figure 1). Therefore, signs of the residual mucosa may be used as a sensitive and specific biomarker indicating the mesenchymal rather than epithelial origin of sinonasal tumours and can facilitate the accurate diagnosis of RMS in combination with other features.

Figure 1.

A 36-year-old female with embryonal RMS, expansive growth centred at ethmoid sinuses and middle nasal concha, orbital involvement and mild enhancement of the tumour. Central and marginal residual mucosa (arrow) was observed.

Figure 2.

A 39-year-old male with pleomorphic RMS, diffuse creeping growth centred at the right ethmoid sinus with orbital involvement, note residual mucosa, central and marginal to the tumour (arrow) significant enhanced on CE-T1WI.

Figure 3.

A 20-year-old male with alveolar RMS centred at the right ethmoid sinus, mainly creeping growth with mild expansive growth. Mild homogeneous enhancement was observed on T1WI; and central and marginal residual mucosa was observed (arrow).

All the 11 cases in this study exhibited bone destruction and multiple sinus involvement. Most of the origin sites of the lesions were located at ethmoid sinuses. The lateral ethmoidal wall (the medial orbital wall) is thin, making orbital cavities prone to the involvement. In this study, 10 cases exhibited tumour invasion into the orbital cavities, and the only embryonal case without orbital invasion originated from the nasopharyngeal-sinonasal interface. Three cases of RMSs showed concurrent orbital and intracranial involvement, with the centres of the lesions located at ethmoid sinuses. Therefore, the orbital cavity is the most frequently invaded non-nasal site of sinonasal RMS, which is consistent with some reports,⁹ and intracranial invasion is the second most frequent finding.

There were one pleomorphic, three alveolar and three embryonal cases of RMS that mainly exhibited characteristics of expansive growth and mass effects through squeezing and displacement of the surrounding bony wall and mucosa (Figure 1). Two embryonal and two alveolar cases showed mainly creeping growth and no expansive mass effect of squeezing (Figure 2). This study did not reveal significant differences among pathological subtypes based on the growth mode.

Tumours of all 11 cases exhibited hypointense signals on T1WI and hyperintense signals on T2WI, compared with the cerebral cortex. Ten cases (91%) exhibited heterogeneous signals, while one alveolar case showed homogeneous signals. All lesions showed mild-to mild-intermediate enhancement on CE-T1WI (using the enhancements of the muscle and mucosa as references), in distinct contrast with the intense enhancement of residual and normal mucosa tissues, which was consistent with some reports.⁹ However, other reports, including that by Yu et al, showed different findings.^7,10,11 The discrepancy may be due to the emphasis on CT features in early studies, as CT results are prone to distortions, due to the pneumaticity of paranasal sinuses.

Early lymphatic metastasis has been reported as one characteristic of RMS of paranasal sinuses.^1,15 In this study, six cases exhibited metastasis to cervical, submandibular and parapharyngeal lymph nodes, with ipsilateral metastasis in four cases and contralateral metastasis to parapharyngeal lymph nodes, in addition to ipsilateral metastasis, in two cases. No haematogenous metastasis was observed in any of the 11 cases. Bone destruction was observed in all 11 cases, including at the sinus walls, nasal conchae and orbital walls. Although MRI is not as straightforward as CT, the loss of hypointense signals of the bone is a reliable marker of bone destruction. MRI is also more sensitive than CT in terms of uncovering mild tumour invasions into the contralateral bony wall.

The nasal RMS should be differentiated from the benign (such as Sinonasal papillomas and meningiomas) or malignant entities (such as lymphoma and paranasal sinus cancers). Sinonasal papillomas are benign epithelial neoplasms, which arise from the Schneiderian mucosa and are histopathologically divided into three subtypes.¹⁶ These tumours are characterized by inverted growth of mucosal epithelial squamous cells or respiratory cells with a multilayered epithelium and an intact basilar membrane. The incidence in males is 2.5- to 3-fold that in females.^17,18 Papillomas frequently show a lobulated shape with hyperintensity on T2W images and iso- to hypointensity on T1W images. A convoluted cerebriform pattern is characteristic of papillomas, showing alternating hypointense and hyperintense bands on T2W images and CE-T1W images, which resemble cerebral gyri.¹⁹ Papillomas are relatively easily distinguishable from RMS. Meningiomas of the sinonasal tract with no direct cranial attachment are extremely rare, whereas secondary sinonasal meningiomas, which show direct extension, are much more common.¹⁹ The primary meningioma tumour commonly presents iso-/hypo-intensity on T2W images and iso-/hypo-intensity on T1W images, with homogeneous contrast enhancement, and bone destruction is not observed as frequently as osteosclerosis. Sinonasal schwannomas arise from branches of cranial nerves (V and IX–XII) and the autonomic nervous system and particularly occur in the ethmoid sinus, followed by the maxillary sinus and nasal cavity. Tumours may expand into the orbit, nasopharynx and cranial cavity,²⁰ which should be differentiated from RMS. Schwannomas exhibit expansive growth and exert pressure on bones, instead of destruction. MRI shows hyperintensity on T2W images and hypointensity on T1W images. Although schwannomas are hypovascular tumours, most cases show marked and delayed contrast enhancement in dynamic studies. Cystic and haemorrhagic changes are common.²¹ Neither tumour exhibits signs of a residual mucosa.

Paranasal sinus cancers are the most common malignant sinonasal tumours and are mainly squamous cell carcinomas, exhibiting homogeneous signals on T1WI, heterogeneous signals on T2WI, marked heterogeneous enhancement, frequent tumour necrosis and clear bone destruction. One recent study showed that a significant difference in ADCs between sinonasal RMS and carcinomas (b value 0, 1000; RMS: 0.992 ± 0.133, carcinomas: 1.259 ± 0.277; p < 0.001) played an important role in differentiation from each other.⁶ Similar findings were reported in another DWI study showing optimized ADC _mean thresholds of 0.79 achieved maximal discriminatory accuracies of 100% for differentiating adenoid cystic carcinoma from sinonasal undifferentiated carcinoma.²² These studies indicated diffusion-weighted imaging (DWI) could be used to differentiate sinonasal cancer from nasal RMS. Lymphomas are the second most common malignant sinonasal tumours.²³ Lymphomas may exhibit bone invasion or remodeling, with no significant bone destruction, no or mild destruction of deep bone structures, homogeneous signals on MRI-T1WI/T2WI and significant homogeneous enhancement.^19,24–29 Taken together, the above-descripted imaging features may be distinguishable from RMS.

Some limitations should be addressed in this study. First, the sample size of this case series is small, and caution must be applied when interpreting the imaging features. Future studies with larger sample sizes of sinonasal RMSs are needed to validate the observed imaging findings in this study. Second, the absence of detailed evaluation in association of imaging features with prognosis and survival weakens the potential clinical value of our findings. Third, although we have tried our utmost to control the possible confounding effects on the imaging assessment, intensive research efforts were needed to rule out the subjectivity from different observers in the process of imaging features recognition.

Conclusion

In summary, sinonasal RMSs are extremely rare and difficult for preoperative diagnosis. Some MRI features may be indicative of the diagnosis of sinonasal RMSs. When a heterogeneous mass in sinonasal regions (especially in ethmoid sinuses and the middle nasal concha) with characteristic residual mucosa, intermediate signal intensity on T2WI, mild enhancement, bone destruction and orbital invasion is encountered, the possibility of a sinonasal RMS should be considered preoperatively.