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AJR 2000; 175:465-468
© American Roentgen Ray Society


Original Report

Potentially Distinctive Features of Sinonasal Inverted Papilloma on MR Imaging

Hiroya Ojiri1, Masuo Ujita, Shimpei Tada and Kunihiko Fukuda

1 All authors: Department of Radiology, Jikei University School of Medicine, 3-25-8 Nishi-shimbashi, Minato-ku, Tokyo 105-8461 Japan.

Received November 2, 1999; accepted after revision January 6, 2000.

 
Address correspondence to H. Ojiri.


Abstract
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. The objective of this study is to describe potentially distinctive MR features of sinonasal inverted papilloma and those of coexisting squamous cell carcinoma.

CONCLUSION. A sinonasal mass with a convoluted cerebriform pattern on T2- or enhanced T1-weighted images suggests inverted papilloma as a histologic diagnosis. Necrosis in a mass with such an appearance strongly suggests coexistent carcinoma.


Introduction
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Fungiform papilloma, inverted papilloma, and cylindric cell papilloma, three distinctive histologic types of nasal papillomas, have been described [1,2,3]. Inverted papilloma accounts for 47% of all nasal papillomas.

MR imaging routinely shows the internal architecture of sinonasal soft-tissue masses. To our knowledge, only one report on MR features of inverted papilloma exists. In this report, Yousem et al. [4] concluded that no signature pattern of MR imaging is suggestive of a specific diagnosis of inverted papilloma. Barnes et al. [5], writing in the pathology literature, described a distinctive gross mucosal morphology of inverted papilloma called a convoluted cerebriform pattern. On physical examination, an inverted papilloma presents as a polypoid growth covered by a convoluted cerebriform mucosa [5]. This distinctive gross morphology, together with the solid cellular nature of its neoplastic and interventing stromal elements, is a unique internal MR feature (Fig. 1A,1B,1C,1D). These features might reflect Barnes' gross description of the superficial aspect of these neoplasms. If such a distinctive MR appearance could be determined, then MR imaging might prevent unnecessary biopsy. Inverted papilloma can be associated with or transition to malignancy. Imaging findings may suggest co-existent squamous cell carcinoma before definitive treatment and may reduce the incidence of 5.5-27% cases of compromised care when carcinoma is not anticipated [4].



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Fig. 1A. —45-year-old man with inverted papilloma. Unenhanced spin-echo T1-weighted coronal MR image (TR/TE, 470/17) shows intermediate-signal-intensity mass that is relatively nondescript in internal architecture and involves right-sided maxillary antrum, nasal cavity, and ethmoidal sinus.

 


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Fig. 1B. —45-year-old man with inverted papilloma. Unenhanced fast spin-echo T2-weighted coronal MR image (4600/120) reveals convoluted cerebriform pattern throughout mass. Pattern consists of low-signal-intensity (arrowheads) and relatively high-signal-intensity (small arrows) striations that probably represent metaplastic squamous epithelium and edematous stroma, respectively. Note mucous-filled gaps between folds of tissue that are difficult to identify with certainty. Secretions after obstruction in lateralmost portion of right-sided maxillary antrum are of extremely high signal intensity (large arrow).

 


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Fig. 1C. —45-year-old man with inverted papilloma. Contrast-enhanced spin-echo T1-weighted coronal MR image (470/17) shows well-enhancing stroma (small arrows) and less-enhancing epithelium (arrowheads) that create convoluted cerebriform pattern correlating with that seen in B. Trapped secretions (large arrow) in lateralmost portion of right-sided maxillary antrum do not enhance.

 


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Fig. 1D. —45-year-old man with inverted papilloma. Photomicrograph of histopathologic specimen shows characteristic inverted morphologic features. Note hyperplastic squamous epithelium (E) protruding into (arrows) stroma (S) producing grossly convoluted cerebriform appearance. G = tissue gap. (H and E, x 5)

 

We retrospectively reviewed MR imaging studies of patients with biopsy-proven inverted papilloma to determine whether a convoluted cerebriform pattern on MR imaging helps characterize these tumors and whether it might help to diagnose coexistent squamous cell carcinoma.


Materials and Methods
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Three radiologists retrospectively reviewed MR images of 10 consecutive (between January 1997 and December 1998) previously untreated patients with biopsy-proven inverted papilloma. These independent interpreters were not aware of the surgical and precise histologic findings. The study population consisted of seven men and three women, 40-73 years old (mean age, 57.6 years). MR imaging was performed on a 1.5-T MR system (Visart; Toshiba Medical, Tokyo, Japan) in three patients; on a 1.0-T MR system (Magnetom Impact; Siemens, Erlangen, Germany) in six patients; and on a 0.5-T MR system (MRT-500; Hitachi Medico, Tokyo, Japan) in one patient. Fast spin-echo T2-weighted pulse sequences were used in nine patients. T1-weighted images were obtained with a TR range/TE range of 450-690/12-21. Fast spin-echo T2-weighted images were obtained with 2500-4600/80-110. Gadopentetate dimeglumine was administered at a dose of 0.1 mmol/kg in nine of 10 patients. A standard head coil was used. Section thickness was usually 3 mm with an intersection gap of 0.5 mm. A typical field of view of 16-18 cm was used for T1-weighted images and 20-24 cm for T2-weighted images.

All 10 patients underwent surgical resection after imaging. Direct gross macroscopic pathologic-radiologic correlation was performed in three patients. The other seven specimens were evaluated by routine microscopic histopathologic techniques.


Results
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Abstract
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Materials and Methods
Results
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Soft-tissue masses involved the middle meatus and maxillary sinus in all 10 patients. The masses enhanced in all nine patients administered contrast material. The tumor had spread to the ethmoidal sinuses in six patients, to the nasopharyngeal cavities in four, and to the orbit in one. Obstructive sinus changes were present in nine patients (two in ethmoidal, four in maxillary, two in sphenoid, and one in the frontal sinus).

The general tumor intensity was isointense (n = 8) or slightly hyperintense (n = 2) to the skeletal muscle on unenhanced T1-weighted images (Fig. 1A) and clearly hyperintense to skeletal muscle in all 10 patients on T2-weighted images (Fig. 1B). Curvilinear hyperintense striations were present throughout the tumor mass in eight patients on T2-weighted and contrast-enhanced T1-weighted images (Fig. 1C). In one of these eight patients, histopathology showed this convoluted cerebriform pattern of striations to be in an inverted papilloma concomitant with multifocal microscopic squamous cell carcinoma. Two other patients with concomitant inverted papilloma and squamous cell carcinoma had a pattern of gross central necrosis, with histopathology revealing a gross focal squamous cell carcinoma surrounding the zone of necrotic material (Fig. 2).



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Fig. 2. —47-year-old man with concomitant inverted papilloma and focal squamous cell carcinoma (pathologic group 2). Contrast-enhanced spin-echo T1-weighted axial MR image (TR/TE, 500/19) reveals inhomogeneously enhancing tumor destroying medial and anterior walls of left-sided maxillary antrum (small arrows). Tumor also directly invades retromaxillary fat pad (arrowhead). Poorly enhancing area (large arrow) in lesion represents gross central necrosis. Because this patient had predominantly squamous cell carcinoma with only small component of inverted papilloma, cerebriform pattern was not identified throughout entire mass as in other patients (Figs. 1A,1B,1C,1D and 3), who had inverted papilloma with or without small foci of coexisting squamous cell carcinoma not identified in this tumor.

 



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Fig. 3. —47-year-old man with concomitant inverted papilloma and squamous cell carcinoma (pathologic group 1). Unenhanced fast spin-echo T2-weighted coronal MR image (TR/TE, 4600/120) discloses intermediate-signal-intensity mass centered in right-sided nasal cavity and maxillary antrum. Convoluted cerebriform pattern is present throughout entirety of mass. Multifocal in situ squamous cell carcinoma was present diffusely in mucosa of this inverted papilloma but did not disturb basic morphologic inverted papilloma pattern. Secondary frontal and ethmoidal obstructive changes are easily differentiated from inverted papilloma.

 
The direct gross pathologic-radiologic correlation in three patients with inverted papilloma alone always revealed that the metaplastic squamous epithelium, loosely fibrous stroma, and intervening gaps between these folds of tissue combined to create this convoluted cerebriform pattern found on the MR images (Fig. 1A,1B,1C,1D). The tissue gaps, however, were difficult to distinguish from stroma on the MR images.


Discussion
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Nasal papillomas are uncommon, accounting for only 0.4-4.7% of all sinonasal tumors [2, 4]. Most recent pathologic descriptions of nasal papillomas refer to distinct forms: namely, fungiform papilloma, inverted papilloma, and cylindric cell papilloma [1,2,3].

Inverted papilloma is the histologic diagnosis in 47% of nasal papillomas [2]. First described by Ward [6] in 1854, the inverted papilloma was characterized by Ringertz [7] in 1938 as one with a propensity for invading the surrounding tissue and for recurrence. Inverted papilloma is a benign epithelial neoplasm of the sinonasal cavity that has a significant malignant potential. Inverted papillomas most often affect patients from 40 to 70 years old and occur two to four times more often in men than in women [2, 5]. The common symptoms are epistaxis, rhinorrhea, nasal obstruction, anosmia, sinusitis, facial pain, and frontal headache. The cause is uncertain [8].

Because the lesion is accessible for biopsy, the diagnosis of inverted papilloma is readily made on histologic examination of the biopsy specimen. Typical histologic changes can be summarized as a patchy severe squamous metaplasia on polypoid protuberances of nasal mucosa and submucosa and within related ductal epithelium. The polypoid protuberances are possibly formed by invagination of surface mucosa within polyps [1, 7] (Fig. 1D).

On gross examination, inverted papilloma appears as a mucosal polypoid lesion [1, 3]. Most arise from the lateral wall of the nasal cavity and sometimes extend centrifugally into maxillary or ethmoidal sinuses [2, 3, 5, 9].

Diagnostic imaging helps to identify a sinonasal mass as likely caused by inverted papilloma, when a polypoid morphology can be identified and the mass seems to arise on the lateral nasal wall. Imaging is also used to establish the extent of inverted papilloma and possibly to anticipate an associated malignancy. A convoluted cerebriform gross morphology was noted on T2- or contrast-enhanced T1-weighted images or both in eight of our 10 patients with inverted papilloma (Figs. 1B and 1C). Yousem et al. [4] described a septate striated appearance in five of 10 patients with inverted papillomas. Those authors suggested that this septate striated appearance was nonspecific because it was also found in one squamous cell carcinoma and one olfactory neuroblastoma in an informal review of eight other sinonasal malignancies in their practice [4]. The convoluted cerebriform appearance that we describe in this article is likely the septate striated appearance mentioned by Yousem et al. No other similar descriptions could be found concerning the imaging appearance of inverted papilloma in textbooks or in other nonpathology literature [4, 5]. This appearance would certainly be expected on the basis of the pathology literature [5].

The direct gross pathologic-radiologic correlation in three patients with inverted papilloma alone also consistently confirmed a convoluted cerebriform pattern (Fig. 1A,1B,1C,1D). On fast spin-echo T2-weighted images this pattern consisted of striations of high signal intensity and other striations that were thinner and closer to fat in signal intensity (Fig. 1B). Correlating with gross histologic sections, the thinner lower signal-intensity striations were considered to correspond to the higher cellular metaplastic epithelium and the thicker higher signal-intensity striations to the less cellular edematous stroma (Fig. 1E). On contrast-enhanced T1-weighted images, it seems that less-enhancing metaplastic squamous epithelium, well-enhancing stroma, and the gaps between these folds of tissue combined, like multiple strands, to create this convoluted cerebriform pattern (Fig. 1C). According to the pathology literature, the stroma of inverted papilloma ranges from compact and fibrous to edematous and loosely fibrous. This range means that the signal intensity or enhancement pattern of the stroma might vary considerably [5]. Whereas constituency of the convolutions might vary internally, the overall cerebriform morphology, in this series, remained a constant feature of isolated inverted papilloma. Although Barnes et al. [5] probably first used the term "convoluted cerebriform" to describe this gross morphologic feature of inverted papilloma, it has not been emphasized as a distinctive radiologic feature of inverted papilloma. Our experience suggests that the convoluted cerebriform pattern may be more specific than suggested in the work by Yousem et al. [4], and it may accurately reflect the internal gross morphology of the lesion and the superficial morphology for which the term was originally coined by Barnes et al.

Three of our patients had squamous cell carcinoma concomitant with inverted papilloma, and gross central necrosis of the entire tumor mass was seen in two patients (Fig. 2). Gross central necrosis was not present in any other patient. The other patient with concomitant inverted papilloma had multiple small foci of squamous cell carcinoma distributed throughout a typical convoluted cerebriform mass that could not be discriminated from inverted papilloma on MR images (Fig. 3). Pathologically, patients with squamous cell carcinoma complicating inverted papillomas have been classified in three groups: group 1, those whose tumors are primarily inverted papillomas with only small foci of in situ or invasive squamous cell carcinoma; group 2, those who have predominantly squamous cell carcinoma with only an incidental or small component of inverted papilloma; and group 3, those who had a history of histologically documented inverted papillomas who subsequently develop a "pure" squamous cell carcinoma in the area where the inverted papilloma occurred [5]. The two patients with inverted papilloma and gross central necrosis could be classified in group 2, and the other patient with multiple small foci of squamous cell carcinoma was classified in group 1.

Patients of either group 1 or group 2 can initially present with a diagnosis of benign inverted papilloma as a result of sampling a histologically benign portion of a combined lesion. Actually, a group 2 lesion is considered the same as squamous cell carcinoma although it contains a small component of inverted papilloma that can be sampled as a biopsy specimen.

The gross morphology of a sinonasal mass, as seen on MR images in a patient with biopsy-proven inverted papilloma, can help warn the surgeon of a probable associated malignancy. Central necrosis in a sinonasal tumor requires consideration of an associated malignancy (group 2) even when the preoperative biopsy is purely inverted papilloma. Radiologists should look for signs of locally invasive disease that might otherwise go unappreciated and greatly alter the surgical approach when a necrotic mass is present (Fig. 2). MR imaging would classify such patients in the pathologic group 2.

Patients whose MR images reveal a typical convoluted cerebriform pattern can have a small foci of in situ squamous cell carcinoma as noted in our third patient with concomitant cancer and inverted papilloma (Fig. 3). MR imaging would help retrospectively classify such patients in the pathologic group 1. In this circumstance, one would predict, from the imaging findings, gross total excision of the inverted papilloma and cancer by the surgery originally planned for the removal of inverted papilloma alone. The imaging then serves to confirm that there is no grossly infiltrative margin that needs to be anticipated by the surgeon, thus increasing the surgeon's degree of confidence in the approach that is chosen. Then depending on the pathologic margins, the patient may be followed up or receive additional treatment.

In summary, a solid tumor occupying the middle meatus and maxillary sinus with a convoluted cerebriform appearance on T2-weighted images or enhanced T1-weighted images strongly suggests the diagnosis of inverted papilloma. When inverted papilloma is the result of a biopsy of a sinonasal mass, deviation from this convoluted cerebriform pattern strongly suggests an alternative diagnosis or concomitant inverted papilloma and squamous cell carcinoma.


Acknowledgments
 
We thank Anthony A. Mancuso for his invaluable help in the revision and correction of this manuscript.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

  1. Michaels L, Young M. Histogenesis of papillomas of the nose and paranasal sinuses. Arch Pathol Lab Med 1995;119:821 -826[Medline]
  2. Som PM, Brandwein M. Tumors and tumorlike conditions: sinonasal cavities—inflammatory diseases, tumors, fractures, and postoperative findings. In: Som PM, Cutin HD, eds. Head and neck imaging, 2nd ed. St. Louis: Mosby, 1996:185 -262
  3. Michaels L. Benign mucosal tumors of the nose and paranasal sinuses. Semin Diagn Pathol 1996;13:113 -117[Medline]
  4. Yousem DM, Fellows DW, Kennedy DW, Bolger WE, Kashima H, Zinreich SJ. Inverted papilloma: evaluation with MR imaging. Radiology 1992;185:501 -505[Abstract/Free Full Text]
  5. Barnes L, Verbin RS, Gnepp DR. Diseases of the nose, paranasal sinuses, and nasopharynx. In: Barnes L, ed. Surgical pathology of the head and neck, vol. 1. New York: Marcel Dekker, 1985:403 -451
  6. Ward N. A mirror of the practice of medicine and surgery in the hospitals of London: London Hospital. Lancet 1854;2:480 -482
  7. Ringertz N. Pathology of malignant tumors arising in the nasal and paranasal cavities and maxilla. Acta Otolaryngol Suppl 1938;27:31 -42
  8. Vrabec DP. The inverted papilloma: a 25-year study. Laryngoscope 1994;104:582 -605[Medline]
  9. DeSanto LW. Neoplasms. In: Cummings CW, Fredrickson JM, Harker LA, Krause CJ, Schuller DE, eds. Otolaryngology—head and neck surgery, 2nd ed. St. Louis: Mosby—Year Book, 1993: 754-764

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