Jpn J Radiol DOI 10.1007/s11604-013-0247-z
ORIGINAL ARTICLE
Adenoid cystic carcinoma of the maxillary sinus: CT and MR imaging findings Hiroki Kato • Masayuki Kanematsu • Kota Sakurai • Keisuke Mizuta • Mitsuhiro Aoki • Yoshinobu Hirose Shimpei Kawaguchi • Akifumi Fujita • Koshi Ikeda • Tomonori Kanda
•
Received: 7 August 2013 / Accepted: 8 September 2013 Ó Japan Radiological Society 2013
Abstract Objective The purpose of this study was to determine whether adenoid cystic carcinomas (ACCs) of the maxillary sinus have features on CT and MR imaging. Materials and methods Nine patients with histopathologically proved maxillary sinus ACCs were included. The growth pattern was classified as expansile or destructive types on the basis of CT images. CT images were also reviewed for adjacent bony defects and MR images were
H. Kato (&) M. Kanematsu K. Sakurai Department of Radiology, Gifu University School of Medicine, 1-1 Yanagido, Gifu 501-1194, Japan e-mail:
[email protected] M. Kanematsu High-level Imaging Diagnosis Center, Gifu University Hospital, Gifu, Japan K. Mizuta M. Aoki Department of Otolaryngology, Gifu University School of Medicine, Gifu, Japan Y. Hirose Department of Pathology, Gifu University School of Medicine, Gifu, Japan S. Kawaguchi Department of Radiology, Gifu Municipal Hospital, Gifu, Japan A. Fujita Department of Radiology, Jichi Medical University School of Medicine, Tochigi, Japan K. Ikeda Department of Radiology, Kansai Medical University, Osaka, Japan T. Kanda Department of Radiology, Hyogo Cancer Center, Hyogo, Japan
reviewed for tumor extension. Fluid accumulation in the ipsilateral maxillary sinus was also assessed. Results The tumors had caused adjacent bony expansion with minimal bony defects in 4 patients whereas those in the remaining 5 patients had caused extensive destruction of adjacent bones comprising the maxillary sinus walls. Nasal cavity invasion was observed in 7 patients, retroantral fat pad invasion in 5, pterygopalatine fossa invasion in 4, and orbital invasion in 3. All 4 expansile ACCs were accompanied by accumulation of a small amount of fluid in the surroundings of the tumors, which was revealed as hyperintensity on T1-weighted images. Conclusion The growth pattern of maxillary sinus ACCs can be classified into an expansile type with minimal bony defects and a destructive type with extensive bony defects. Keywords Adenoid cystic carcinoma Maxillary sinus MRI CT
Introduction Adenoid cystic carcinomas (ACCs) account for 4–8 % of all salivary gland tumors. They arise from the major and minor salivary glands, sinonasal tract, and tracheobronchial system. ACCs are slowly progressive and widely infiltrative tumors with a propensity for perineural spread along the cranial nerves that can proceed into the skull base. The most common presenting symptom of ACCs is a mass or swelling, and the duration of symptoms before diagnosis varies; the average is 2 years [1]. Recurrence and metastasis can occur decades after treatment of the primary tumor [2]. ACCs are the most common malignant salivary gland tumors in the sinonasal tract, and account for 10 % of all
123
Jpn J Radiol
malignancies at this site [3]. Sinonasal ACCs account for 10–25 % of all head and neck ACCs [4], and the average age at presentation is the fifth to sixth decade [2–5]. The maxillary sinus is the most commonly affected primary site, followed by the nasal fossa, ethmoid sinus, and sphenoid sinus [3]. Sinonasal ACCs tend to have an insidious onset, as with other sinonasal tumors, and most patients have advanced disease on initial evaluation [2]. In addition to a mass, nasal obstruction, nasal bleeding, and pain are commonly observed on presentation [3, 5, 6]. CT findings of ACCs of the sinonasal tract have been described in previous studies [7, 8], but these studies included different types of sinonasal malignancy. MR imaging findings of maxillary sinus ACCs have been reported in one radiological report of head and neck ACCs [9] and in several clinical case reports [6, 10, 11]. However, we failed to find any reports of imaging findings that focused on maxillary sinus ACCs. Therefore, we performed a study wherein we evaluated the CT and MR imaging findings of patients with ACCs of the maxillary sinus and determined whether ACCs of the maxillary sinus have features on CT and MR imaging.
Materials and methods Patients The study was approved by the human research committee of our institutional review board, and complied with the guidelines of the Health Insurance Portability and Accountability Act. The requirement for informed consent was waived because of the retrospective nature of the study. Nine patients diagnosed with histopathologically confirmed ACCs of the maxillary sinus (age 46–78 years; mean 60 years; 4 men and 5 women) between November 2003 and November 2011 were identified in 5 institutions. Histopathological diagnosis was established by surgical excision for all patients. CT and MR imaging were performed for all patients. Three patients complained of painless swelling, 3 of nasal bleeding, 3 of nasal obstruction, 3 of pain, and 1 of cranial nerve paralysis. The predominant histopathological ACC subtypes were cribriform for 5 patients, tubular for 3, and solid for 1. Clinical stages of maxillary sinus ACCs, according to Union for International Cancer Control (UICC) classification, were stage II for 2, stage III for 4, and stage IV for 3. CT and MR imaging MR imaging was performed for all patients using 1.5-T MR imaging systems (GE Healthcare, Siemens, or Philips).
123
Imaging settings differed among the 9 patients, because MR images were obtained at different institutions. MR images were obtained in both transverse and coronal planes. T1-weighted spin-echo (TR/TE, 417–827/9–10 ms; slice thickness, 4–5 mm) and T2-weighted fast spin-echo (TR/TE, 3,000–4,102/90–102 ms; slice thickness 4–5 mm) images were obtained for all patients. Gadoliniumenhanced fat-suppressed T1-weighted spin-echo (TR/TE, 400–730/9–10 ms; slice thickness, 4–5 mm) images were obtained for 7 of the 9 patients. CT imaging was performed for all patients using multidetector row CT systems (GE Healthcare, Siemens, or Toshiba). CT images reconstructed by use of standard and bone algorithms were obtained in both the transverse and coronal multiplanar reformatted images with a slice thickness of 2.5–3 mm. Contrast-enhanced CT images were obtained for 7 of the 9 patients. Image review Two radiologists with 14 and 10 years of post-training experience of head and neck imaging independently reviewed images and any disagreements were resolved by consensus. The growth pattern was classified as expansile and destructive type on the basis of CT images. CT images were also reviewed for adjacent bony defect of maxillary sinus wall and presence of calcification, whereas MR images were reviewed for size, tumor margin, tumor extension, perineural spread, signal intensity within tumors, and intratumoral enhancement. An expansile-type tumor was defined as a non-invasive lesion accompanied by expansion and erosion of adjacent maxillary sinus walls whereas a destructive-type tumor was defined as an invasive lesion accompanied by extensive destruction and no expansion of adjacent maxillary sinus walls. Perineural spread was defined as invasion of the pterygopalatine fossa, followed by extension to the greater or lesser palatine foramen, vidian canal, foramen rotundum, or cavernous sinus. The following diagnostic criteria used for perineural spread were: asymmetric enlargement or destruction on CT images, obliteration of the fat plane on T1-weighted images, or abnormal enhancement on gadolinium-enhanced fat-suppressed T1-weighted images in the greater or lesser palatine foramen, vidian canal, or foramen rotundum. The reviewers also recorded the presence and MR signal intensity of fluid accumulation in the ipsilateral maxillary sinus. Statistical analysis All statistical analysis was performed using SPSS version 18.0 (SPSS, Chicago, Illinois, USA). The unpaired t test was used to compare size between expansile and destructive-type ACCs. The chi-squared test or Fisher’s exact test
Jpn J Radiol
was performed to compare the frequency of evaluated imaging findings between expansile and destructive-type ACCs. The null hypotheses of no difference was rejected if p-values were \0.05.
Results The imaging findings of ACC of the maxillary sinus are summarized in Table 1. Four (44 %) tumors were classified as expansile type (Fig. 1), the remaining 5 (56 %) as destructive type (Fig. 2). The predominant histopathological subtype in 2 of the 4 expansile-type tumors was Table 1 Imaging findings of adenoid cystic carcinoma of the maxillary sinus Growth pattern
Expansile
Destructive
Total
Number of patients
4
5
9
Mean
5.1
4.1
4.5
Range
4.2–6.2
3.6–4.5
3.6–6.2
Maximum diameter (cm)
Predominant histological subtype Solid
0
1
1 (11 %)
Cribriform Tubular
2 2
3 1
5 (56 %) 3 (33 %)
Adjacent bony defect of maxillary sinus wall No
0
0
0 (0 %)
Minimal
4
0
4 (44 %)
Extensive
0
5
5 (56 %)
Calcification
0
0
0 (0 %)
Tumor margin Well-demarcated
4
1
5 (56 %)
Ill-demarcated
0
4
4 (44 %)
Tumor extension Nasal cavity
4
3
7 (78 %)
Retroantral fat pad
3
2
5 (56 %)
Pterygopalatine fossa
2
2
4 (44 %)
Orbit
1
2
3 (33 %)
Pterygoid process Cavernous sinus
0 0
1 1
1 (11 %) 1 (11 %)
2
2
4 (44 %)
Perineural spread
Predominant intensity on T2-weighted image Isointensity
2
4
6 (67 %)
Hyperintensity
2
1
3 (33 %)
Intratumoral enhancement (n = 7) Heterogeneous enhancement
4
3
7
Intratumoral unenhanced area
4
2
6 (86 %)
cribriform whereas that in the other 2 was tubular. The predominant histopathological subtype in 3 of the 5 destructive-type tumors was cribriform whereas that in the others was tubular and solid. All 4 expansile-type tumors had caused minimal bony defects. Calcification was not observed within the tumors on unenhanced CT. The maximum diameter of the tumors ranged from 3.6 to 6.2 cm (mean 4.5 cm). All expansile-type ACCs had welldemarcated margins whereas 4 of 5 destructive-type ACCs had ill-demarcated margins. Nasal cavity invasion was observed in 7 (78 %) patients, retroantral fat pad invasion in 5 (56 %), pterygopalatine fossa invasion in 4 (44 %), orbital invasion in 3 (33 %), pterygoid process invasion in 1 (11 %), and cavernous sinus invasion through the foramen rotundum in 1 (11 %). Perineural spread was observed in 4 (44 %) patients. On T1-weighted images, all tumors were heterogeneously hypointense compared with the cerebral gray matter; spotty hyperintensity was observed for 3 tumors (33 %). On T2-weighted images, all tumors had heterogeneous signal intensity and were predominantly isointense or hyperintense compared with the cerebral gray matter. Fluid– fluid levels within the tumor were observed for one patient. On T2-weighted images, 4 of the 5 cribriform ACCs and 1 solid ACC were predominantly isointense compared with the cerebral gray matter, and 2 of the 3 tubular ACCs were predominantly hyperintense. Solid components of the tumors were heterogeneously enhanced, and intratumoral unenhanced areas that corresponded to cystic degeneration or necrosis were observed in 6 (86 %) of the 7 tumors. All 4 expansile-type tumors were accompanied by ipsilateral maxillary sinus fluid accumulation that appeared hyperintense on T1-weighted images and isointense to hypointense on T2-weighted images. On T1-weighted images, compared with the muscle, the maxillary sinus fluid was extremely hyperintense for 3 patients and slightly hyperintense for 1. The small amount of hyperintense fluid on T1-weighted images was located in the surroundings of the expansile-type tumors occupying the maxillary sinus for all 4 patients. No significant difference was found between the sizes of expansile-type tumors (40.6 ± 3.3 mm) and destructivetype tumors (50.8 ± 9.1 mm) (p = 0.11). The frequency of minimal bony defects, well-demarcated margins, nasal cavity invasion, and ipsilateral maxillary sinus fluid was significantly higher for expansile-type tumors than for destructive-type tumors (p \ 0.01). No significant difference was found for other imaging findings between expansile and destructive-type ACCs.
(100 %)
Discussion
Fluid of ipsilateral maxillary sinus Hyperintensity on T1weighted image
4
0
4 (44 %)
The histopathological subtypes of ACCs are classified into 3 distinct patterns: tubular/tubuloductal, cribriform, and
123
Jpn J Radiol
Fig. 1 A 46-year-old man with expansile ACC of the left maxillary sinus (tubular subtype). a Unenhanced CT image shows an expansile maxillary sinus tumor (arrow) with minimal bony defects of the anterior maxillary sinus wall (curved arrow). Peripheral rim-like and septal-like hyperdense areas are observed (arrow heads). b Unenhanced CT image reconstructed by use of the bone algorithm shows expansion of the posterior maxillary sinus wall (arrow) and minimal bony defects of the anterior maxillary sinus wall (arrow head). c Contrast-enhanced CT image shows an expansile maxillary sinus tumor (arrow) with heterogeneous enhancement and invasion of the nasal cavity. d T2-weighted fast spin-echo MR image (TR/TE, 4,102/
90 ms) shows a heterogeneous hyperintense tumor (arrow) accompanied by fluid–fluid level formation (curved arrow). A small amount of hypointense fluid is observed in the surroundings of the tumor (arrow head). e T1-weighted spin-echo MR image (TR/TE, 827/9 ms) shows a hypointense tumor (arrow). Peripheral rim-like and septal-like hyperintense areas (arrow heads) are suggestive of fluid accumulation in the surroundings or gaps of the multinodular tumor (arrow). f Fat-suppressed gadolinium-enhanced T1-weighted spin-echo MR image (TR/TE, 730/9 ms) shows a heterogeneously enhanced tumor (arrow) with unenhanced areas (arrow heads)
solid subtype. The cribriform subtype is the most common whereas the solid subtype is the least common. Prognosis of the solid subtype is the worst whereas that of the tubular subtype is the best. The tubular subtype is difficult to interpret because some physicians believe it to be similar to the cribriform subtype in behavior. The cribriform subtype contains clusters and nests of epithelial cells with holes (spaces) whereas the solid subtype contains tumor cells arranged in nests with larger basaloid cells, pleomorphism, and prevalent mitoses. All 3 types have a tendency for perineural invasion. In our series, one solid ACC was the destructive type whereas 2 of 3 tubular ACCs were expansile type. Therefore, imaging features might reflect histopathological aggressiveness. ACCs may appear as either a benign or malignant process on imaging. Because MR findings of ACCs are not specific, histopathological examination must ensure correct diagnosis. On T2-weighted images, lesions with hypointensity corresponded to highly cellular tumors (solid
subtype) whereas lesions with hyperintensity were less cellular tumors (cribriform or tubular subtype) [9]. MR imaging is more sensitive than CT for detection of perineural tumor invasion, and enlarged nerves with enhancement can be identified on contrast-enhanced MR images [12, 13]. The diagnostic value of 18F-fluorodeoxyglucose (FDG) PET/CT for ACCs is limited because the metabolic activity of and, consequently, FDG uptake by these tumors are low [14]. Different imaging findings are also observed for ACCs arising from the nasal cavity and the paranasal sinus. Lowgrade sinonasal ACCs may present as a polypoid lesion that remodels bone and mimics a simple polyp whereas high-grade sinonasal ACCs may present as large irregular masses with bone destruction and heterogeneous density or signal intensity [15]. Sinonasal ACCs usually destroy the bones comprising the maxillary wall, sometimes the pterygoid plate and orbital wall, and occasionally the skull base [7].
123
Jpn J Radiol
Fig. 2 A 60-year-old woman with destructive ACC of the left maxillary sinus (cribriform subtype). a Unenhanced CT image shows an opacified sinus (arrow) with destructive maxillary sinus tumor (arrow heads). b Unenhanced CT image reconstructed with bone algorithm shows an extensive bony defect of the posterior maxillary sinus wall (arrow head). c Contrast-enhanced CT image shows a destructive maxillary sinus tumor (arrow) with pterygopalatine fossa invasion accompanied by perineural spread (arrow head). d T2weighted fast spin-echo MR image (TR/TE, 4,102/90 ms) shows a
heterogeneous isointense tumor (arrow) with central necrosis (arrow head). Nasal cavity invasion is not observed. e T1-weighted spin-echo MR image (TR/TE, 827/9 ms) shows a hypointense tumor (arrow) with pterygopalatine fossa invasion accompanied by perineural spread (arrow head). f Fat-suppressed gadolinium-enhanced T1-weighted spin-echo MR image (TR/TE, 730/9 ms) shows a necrotic tumor (arrow) with invasion along the zygomatic bone (curved arrow). Pterygopalatine fossa invasion accompanied by perineural spread is observed (arrow head)
Although we classified the radiological growth pattern of maxillary sinus ACCs into expansile and destructive types, we could not clarify the relationship between radiological growth pattern and histopathological subtype. This is because combinations of the 3 histopathological subtypes are often encountered in single neoplasm. In a patient in our series, although the cribriform subtype was predominant, the radiological growth pattern was expansile because of the histopathologically proved tubular subtype located adjacent to maxillary sinus walls. In our series, all 4 expansile ACCs of the maxillary sinus were accompanied by ipsilateral maxillary sinus fluid accumulation which appeared hyperintense on T1-weighted images and isointense to hypointense on T2-weighted images. This characteristic imaging finding was not found for any of the destructive ACCs of the maxillary sinus. We assumed that the concentration of mucous secretion or hemorrhage might cause hyperintense fluid accumulation on T1-weighted images because of the slow-growing nature of expansile ACCs.
The differential diagnosis of maxillary sinus ACCs includes many other histological types. Although it is difficult to distinguish destructive ACCs from squamous cell carcinoma (SCC) and lymphoma by conventional imaging, diffusion-weighted MR images may be useful to distinguish lymphoma from other malignancies. SCCs accounts for 80 % of all malignant tumors of the sinonasal tract, and most sinonasal SCCs arise in the maxillary sinus. Maxillary sinus SCC appears as a unilateral sinus mass with aggressive bone destruction on CT, and may involve the alveolar ridge of the maxilla, buccal space, and hard palate. Lymphoma of the sinonasal tract often has a highly aggressive appearance with local bone destruction or skull base invasion, and imaging may provide clues to diagnosis on the basis of extensive involvement of the extrasinus soft tissues, the involvement of multiple sites, and/or the presence of cervical lymphadenopathy. Although differential diagnoses of expansile ACCs include mucocele and inverted papilloma with slow-growing nature, the hyperintense fluid in the surroundings of the tumors on T1-
123
Jpn J Radiol
weighted images may be a diagnostic radiological clue to the correct differentiation of expansile ACCs. This study has several limitations. First, because the study population was small, we need to clarify the imaging findings in larger population-based studies. However, we believe that we could assess a variety of imaging findings of maxillary sinus ACCs. To summarize, the growth pattern of maxillary sinus ACCs can be classified into an expansile type with minimal bony defects and a destructive type with extensive bony defects. These tumors usually extend to the nasal cavity and occasionally extend to the retroantral fat pad, pterygopalatine fossa, or orbit. Perineural spread was occasionally encountered. The small amount of hyperintense fluid accumulation in the surroundings of the expansile-type tumors observed on T1-weighted images may reflect mucous secretion or hemorrhage because of the slowgrowing nature of expansile-type maxillary sinus ACCs. Conflict of interest of interest.
The authors declare that they have no conflict
References 1. Eby LS, Johnson DS, Baker HW. Adenoid cystic carcinoma of the head and neck. Cancer. 1972;29(5):1160–8. 2. Wiseman SM, Popat SR, Rigual NR, Hicks WL, Jr., Orner JB, Wein RO, et al. Adenoid cystic carcinoma of the paranasal sinuses or nasal cavity: a 40-year review of 35 cases. Ear Nose Throat J. 2002;81(8):510–4, 16–7. 3. Lupinetti AD, Roberts DB, Williams MD, Kupferman ME, Rosenthal DI, Demonte F, et al. Sinonasal adenoid cystic carcinoma: the M.D. Anderson Cancer Center experience. Cancer. 2007; 110(12):2726–31.
123
4. Rhee CS, Won TB, Lee CH, Min YG, Sung MW, Kim KH, et al. Adenoid cystic carcinoma of the sinonasal tract: treatment results. Laryngoscope. 2006;116(6):982–6. 5. da Cruz Perez DE, Pires FR, Lopes MA, de Almeida OP, Kowalski LP. Adenoid cystic carcinoma and mucoepidermoid carcinoma of the maxillary sinus: report of a 44-year experience of 25 cases from a single institution. J Oral Maxillofac Surg. 2006;64(11):1592–7. 6. Muhtaseb M, Ferguson V, Nigar E. Maxillary antral adenoid cystic carcinoma: an unusual presentation. Eye (Lond). 2001;15(Pt 3):354–6. 7. Kondo M, Horiuchi M, Shiga H, Inuyama Y, Dokiya T, Takata Y, et al. Computed tomography of malignant tumors of the nasal cavity and paranasal sinuses. Cancer. 1982;50(2):226–31. 8. Parsons C, Hodson N. Computed tomography of paranasal sinus tumors. Radiology. 1979;132(3):641–5. 9. Sigal R, Monnet O, de Baere T, Micheau C, Shapeero LG, Julieron M, et al. Adenoid cystic carcinoma of the head and neck: evaluation with MR imaging and clinical-pathologic correlation in 27 patients. Radiology. 1992;184(1):95–101. 10. Perusse R. Adenoid cystic carcinoma of the maxillary sinus. J Am Dent Assoc. 1997;128(11):1551–5. 11. Oates JA, Kinsella DC, Gutowski NJ. Neurological picture. Fastgrowing adenoid cystic carcinoma: a neurotropic malignancy. J Neurol Neurosurg Psychiatry. 2006;77(9):1039. 12. Caldemeyer KS, Mathews VP, Righi PD, Smith RR. Imaging features and clinical significance of perineural spread or extension of head and neck tumors. Radiographics. 1998;18(1): 97–110; quiz 47. 13. Shimamoto H, Chindasombatjaroen J, Kakimoto N, Kishino M, Murakami S, Furukawa S. Perineural spread of adenoid cystic carcinoma in the oral and maxillofacial regions: evaluation with contrast-enhanced CT and MRI. Dentomaxillofac Radiol. 2012;41(2):143–51. 14. Jeong HS, Chung MK, Son YI, Choi JY, Kim HJ, Ko YH, et al. Role of 18F-FDG PET/CT in management of high-grade salivary gland malignancies. J Nucl Med. 2007;48(8):1237–44. 15. Eggesbo HB. Imaging of sinonasal tumours. Cancer Imaging. 2012;12:136–52.
