https://doi.org/10.1007/s11282-020-00470-x CASE REPORT
An unusual case of melanoma metastasis in the buccal space: learning by mistakes to distinguish it from salivary neoplasms
P. Grillo1 · A. P. Savoldi1 · R. Di Meo1 · G. Granata1 · G. M. Rodà1 · G. Arrigoni2 · A. M. Saibene3 · G. Franceschelli4 · F. Patella4 · M. Cariati4
Received: 16 October 2019 / Accepted: 21 July 2020 / Published online: 9 August 2020
© The Author(s) 2020
Abstract
Background The buccal space is an unusual location of malignancies. We report here the case of a woman with a melanoma metastasis in buccal fat pad, to evaluate the imaging features which might lead to the correct, although uncommon, diagnosis.
Case presentation A 71-year-old woman presented with a painless visible swelling of the left cheek. MRI revealed the pres- ence of a solid lesion located in the buccal fat pad with features suggestive of malignancy. It showed T1 hyperintensity and T2 hypointensity, and restriction of diffusion. Histological examination showed neoplastic cells compatible with melanoma.
Discussion The lesion features (T1 hyperintensity and T2 hypointensity) initially lead our team to believe that there was a hemorrhagic component, possibly a residue of the biopsy. However, when associated with other malignancy features, such as low apparent diffusion coefficient (ADC) values and contrast enhancement, they should evoke the suspect of melanoma, provided that no biopsy was performed and no trauma occurred in the 3–7 days before.
Keywords Melanoma metastasis · MRI features · Melanoma · Buccal fat pad Abbreviations
ADC Apparent diffusion coefficient CT Computed tomography DWI Diffusion-weighted imaging FNAB Fine-needle-aspiration biopsy LN Lymph node
MRI Magnetic resonance imaging PA Pleomorphic adenoma STIR Short-TI inversion recovery T1w T1-weighted
T2w T2-weighted
Introduction
The buccal space is one of the deep anatomical compart- ments of the head and neck regions, enveloped by the super- ficial layer of the deep cervical fascia (Fig. 1). It is delimited medially by the buccinator muscle, laterally by the platysma muscle, anteriorly by the mimic muscles, and posteriorly by the mandible, medial and lateral pterygoid muscles, and parotid and masseter muscle [1, 2].
Most of the buccal space is occupied by adipose tissue—
the buccal fat pad—which laterally follows the parotid duct ending near the anterolateral portion of the parotid gland;
medially, it projects towards the mandible and maxillary sinus; superiorly, it is divided by the temporal muscle into a superficial and deep portion and by the parotid duct into an anterior and posterior portion [3].
The buccal space frequently communicates with the pos- terior masticatory space and with the infratemporal space;
moreover, there is no real lower boundary with the subman- dibular space. This anatomical space can thus function as a conduit to spread infectious or tumoral tissue between the mouth and the parotid gland.
Buccal space lesions are usually associated with cheek mass or facial swelling [4].
* P. Grillo
pasgrillo1@gmail.com
1 School of Radiodiagnostics, University of Milan, Via Festa del Perdono 7, 20122 Milan, Italy
2 Unit of Pathology, IRCCS San Raffaele Scientific Institute, Milan, Italy
3 Otorhinolaryngology Unit, San Paolo Hospital, Via A. di Rudinì 8, 20142 Milan, Italy
4 Diagnostic and Interventional Radiology Service, San Paolo
Beside inflammatory manifestations and developmental lesions such as accessory parotid tissue (present in up to 20% of the population), dermoid cysts, and vascular mal- formations, a variety of tumors can occur in the buccal space [5].
The most common tumor processes localized in this area arise from minor salivary glands such as pleomor- phic adenoma (PA), adenoid cystic carcinoma, acinic cell carcinoma, and mucoepidermoid carcinoma. Other tumors can originate from connective, muscular, neural, and lym- phatic tissue, such as rhabdomyosarcomas and neurofi- bromas [5].
Metastatic lesions in this region are a very rare occur- rence, accounting for less than 1% of oral cavity malignan- cies [6]. They are most commonly located in bony struc- tures, particularly the mandible, while only about 33% are found in soft tissues [7]. Metastatic lesions can often be the first sign of a widespread malignant disease, generally indicating poor outcome [8]. However, there are only a few studies focusing on metastatic lesions in the buccal and masticatory space, and even less literature regarding malignant melanoma metastases in this region; moreover, most studies were carried out from a surgical standpoint [9–13].
We report here the case of a female patient, with nega- tive oncological history, who presented to our unit with a swelling of the left cheek, which revealed to be a mela- noma metastasis only after surgical exeresis.
We analyze our experience with a revision of the litera- ture, aiming for a retrospective evaluation of the diagnostic imaging characteristics which might be useful in guid- ing the differential diagnosis, to set an example to avoid repeating the same error in the future and to be of help to those who will find themselves in such a situation.
Case report
A 71-year-old woman presented with a painless visible swelling of the left cheek. Skin and oral mucosa were intact and of normal color. At palpation, the mass was mobile and apparently not adherent to the cutaneous and mucosal tissue.
For what concerns comorbidities, the patient was only known for Hashimoto thyroiditis in hormone replacement treatment (no relevant comorbidity was known).
Under ultrasound guidance, a 3-cm hypoechoic lesion was visualized in the left malar region and fine-needle- aspiration biopsy (FNAB) was performed. Cytological examination showed numerous Red Blood Cells, some lymphoid small B- and T-cells, plasma cells with no poly- clonal atypia and a population of small-sized cells with plasmacytoid cells with the following immunophenotype:
S-100 protein + , GFAP ± , P63 ± , cytokeratin7-, suggest- ing a salivary origin. However, a more precise diagnosis was not possible because of the small amount of material available.
The following month, Magnetic Resonance Imag- ing (MRI) with intravenous paramagnetic contrast (Gadobutrol) was performed (Fig. 1). T1-weighted (T1w), T2-weighted (T2w), fat-saturated Short-TI Inver- sion Recovery (STIR), Diffusion-Weighted Imaging (DWI), and T1w sequences after contrast administration were acquired. It revealed the presence of a solid poly- lobate lesion located around the left parotid duct, with an antero-inferior component of 13 × 13 × 15 mm in the soft tissues adjacent to the buccinators, and another com- ponent of about 22 × 27 × 29 mm in the buccal fat pad (Fig. 2) extending into the infratemporal fossa up to the pterygo-maxillary fissure, which exerted a mass effect on
Fig. 1 Anatomy of the buccal space
the masticatory muscles and the posterolateral wall of the maxillary sinus. The mass showed contrast medium uptake and diffusion restriction (apparent diffusion coef- ficient, ADC = 0.9). Notably, the lesion displayed hyper- intense signal compared to muscles in T1w sequences and hypointensity on T2w sequences. Some enlarged oval lymph nodes with progressive contrast enhancement were present in the left fifth cervical level. Overall, the MRI findings were suggestive of a malignant lesion that the
radiologists assumed to have arisen from minor salivary glands on the basis of the anamnesis of the patient and of the epidemiology of neoplasms in this region.
The T1 hyperintensity was referred to possible blood residues in consideration of the recent bioptic procedure.
Surgical exeresis was performed 2 weeks later. Intraoral access through the gingival fornix was obtained. The lesion, which extended to the pterygo-maxillary fis- sure, did not adhere to the surrounding tissues and was
Fig. 2 Magnetic resonance imaging revealed a solid mass located in the left buccal space. a The lesion (arrow) showed a focal component with high signal intensity on axial T1-weighted imaging and b low signal intensity on T2-weighted imaging and c on fat-saturated T2 STIR sequences. d Diffu- sion-weighted imaging revealed a restricted diffusion change with e low apparent diffusion coefficient of 0.9. f After intra- venous contrast administration, the lesion showed increased signal intensity on T1-weighted imaging
easily removed. It was partially solid, with a colliquated component.
Histological examination showed the presence of fibro- connective and lymphatic tissue containing malignant neo- plastic cells compatible with a nodule of melanoma inside the buccal fat pad (Fig. 3).
Gene mutation analysis for c-KIT and BRAF was per- formed: c-KIT was Wild Type (WT), while V600 mutation of BRAF exon 15 was found.
[F-18]FDG PET-CT (Fig. 4) revealed multiple localiza- tions of pathological radiotracer hyper-accumulation: bilat- eral suprahyoid and axillary lymph nodes, fifth liver seg- ment, right adrenal gland, multiple abdominal solid lesions (perigastric, left psoas muscle, right iliac fossa), various subcutaneous, and muscular tissue localizations (left and right thigh and gluteus, right pectoral muscle, right masseter, and right fourth toe).
Full-body computed tomography (CT) with intravenous contrast was then performed, with the following results: no encephalic lesions; 2-cm left cervical lymph node (LN);
5-mm left paracardiac micronodule; 7-cm LN conglomerate in the left axillary region; bilateral adrenal lesions (3.5 cm on the right side; 2 cm on the left); multiple enlarged mes- enteric LNs, the largest of about 2 cm; 2.8-cm lesion in the left psoas muscle.
Dermatological examination revealed a 2-cm ulcerated cutaneous lesion on the distal phalanx of the left fifth fin- ger, compatible with a primitive localization. The patient reported having it for about 1 year but never investigating it.
Incisional biopsy of the lesion was performed, and histologi- cal examination confirmed the presence of melanoma cells with V600E mutation of BRAF gene.
Immediately afterwards, treatment was begun with Dab- rafenib 300 mg/die and Trametinib 2 mg/die.
Fig. 3 Microscopic pictures of the surgical specimen.
a–d H&E stain at increas- ing magnification (respec- tively, × 40, × 100, × 200, and × 400) showing proliferating atypical cells containing coarse- brownish granules suspected to be melanin; e, f, respectively, S-100 and SOX10 immunohis- tochemical stains confirming the diagnosis of melanoma
Two follow-up full-body CTs at 2 and 6 months were per- formed and showed significant size reduction of the axillary and abdominal LNs, of the adrenal and mesenteric localiza- tions, and disappearance of the thoracic nodules.
Discussion
A variety of processes can occur in the buccal space, such as infections, developmental lesions, and tumoral processes.
Neoplastic lesions in this area origin most commonly from minor salivary glands, such as pleomorphic adenoma, adenoid cystic carcinoma, acinic cell carcinoma, and mucoepidermoid carcinoma.
The most frequent benign glandular tumor is PA, which consists of both mesodermal and glandular tissue [3]. It has smooth, rounded margins and shows low signal intensity on T1w image, high T2 signal intensity, and no diffusion restriction on DWI.
The most common malignant glandular tumor is adenoid cystic carcinoma. Some authors have suggested that lesions with low or intermediate T2-hyperintensity or invading
surrounding tissues tend to be more aggressive, whereas lesions characterized by high signal intensity in T2w sequences have lower cellularity and better prognosis [14].
Other tumors can originate from connective, muscular, neural, and lymphatic tissue, such as rhabdomyosarcomas and neurofibromas [5]; rhabdomyosarcomas appear as mus- cle density masses at CT and are hyperintense relative to muscles on T2w MRI often showing bone destruction [15], while neurofibromas show low intensity on T1w imaging and high intensity on T2w imaging and are often associated with neurofibromatosis. Single neurofibromas characteris- tically show the target sign with peripheral hyperintensity [15].
Usually, in diffusion-weighted MRI, the ADC of malig- nant neoplasms of the head and neck regions is lower than that of benign tumors, and it is an important tool in guiding the diagnostic process [16].
Metastatic malignant melanoma is an uncommon head and neck neoplasm. The most frequent localizations of mela- noma metastases are lymph nodes (73.6%), lungs (71.3%), liver (58.3%), brain (49.1%), bone (48.6%), heart (47.2%),
Fig. 4 [F-18]FDG PET-CT reveals avid FDG uptake by the left buccal space lesion (a). Multiple pathological radiotracer hyper-accumulation localizations were present, such as in a voluminous left axillary lymph node (b), a perigastric solid lesion (c), and in the mus- cular tissue of the left thigh (d)
adrenal glands (46.8%), and gastrointestinal tract (43.5%) [17].
Melanoma localized in the oral cavity and surrounding anatomical regions, such as the buccal fat pad, accounts for 0.2–8% of the total cases of melanomas of the body [18].
However, most studies focus on primary malignant mela- noma, while secondary localization of melanoma in this region has been very rarely reported in the literature, with only one study describing a metastatic melanoma in the tongue and, to the best of our knowledge, no reports at all of the secondary melanomas in the buccal space [19].
Therefore, based on epidemiologic criteria, it is rather hard to diagnose metastatic melanoma in the buccal space in patients with an unknown primary tumor, as in our case.
Yet, MRI may be helpful in the identification of mela- noma metastases [20].
Two main MRI patterns of melanoma can be identified:
a melanocytic and amelanocytic pattern [21].
Lesions showing a melanocytic pattern, which is the more common one, are characterized by signal hyperintensity in T1w and hypointensity in T2w images. This is due to the presence of melanin and blood products inside the lesion, although some authors argue that the T1 hyperintensity is more relevantly associated with the presence of blood prod- ucts [21–23].
Less commonly, malignant melanoma may show an amelanocytic (and therefore a specific) pattern, character- ized by hypo- or isointensity in T1w images and hyper- or isointensity in T2w images [21], which is associated at histo- pathological examination to lower quantity of melanin inside the lesion [24].
Macroscopically, metastatic malignant melanoma may present in different ways, ranging from small rapidly grow- ing lesions which may initially go undetected or misrecog- nized as artifacts, to showing a military pattern [25].
In our case, MRI showed a single lesion that exhibited diffusion restriction with ADC of 0.9 and high contrast medium uptake, characteristics suggestive of malignancy as it was proposed in the report.
Moreover, the mass was characterized by T1 hyperinten- sity and T2 hypointensity, a behavior which may be attrib- uted to the melanoma melanocytic pattern; however, it is not specific, since such features may be ascribed to other paraphysiological and pathological processes, including hemorrhages and proteinic fluid collections.
In this case, radiologists supposed that there was a hem- orrhagic component inside the lesion, possibly a residue of the FNAB which had been performed 1 month and a half before. Yet, this was a mistake. In fact, only early subacute hemorrhage dating 3–7 days is featured by T1 hyperintensity and T2 hypointensity, whereas chronic hemorrhages dating more than 1 month are rather characterized by both T1 and T2 hypointensity (26).
Overlooking this aspect and ignoring a part of the anam- nesis, radiologists assumed that they were dealing with a primitive buccal space neoplasm, namely with a malignant (minor) salivary gland tumor.
On the contrary, this case teaches that T1 hyperintensity and T2 hypointensity, when associated with other malig- nancy features in buccal space lesion such as low ADC values and contrast enhancement, should always evoke the suspicion of melanoma, provided that no biopsy was per- formed and no trauma occurred in the 3–7 days before MRI examination.
Acknowledgements Open access funding provided by Università degli Studi di Milano within the CRUI-CARE Agreement.
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Conflict of interest The authors declare that they have no conflict of interest.
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