High-Resolution MRI of Basal Cell Carcinomas of the Face Using a Microscopy Coil

Transcription

1 MRI of Basal Cell Carcinomas of the Face Head and Neck Imaging Clinical Observations Hubert Gufler 1 Folker E. Franke 2 Wigbert S. Rau 1 Gufler H, Franke FE, Rau WS Keywords: head and neck imaging, high resolution, MRI, MR technique, soft-tissue neoplasms DOI: /AJR Received May 10, 2005; accepted after revision April 11, Department of Diagnostic Radiology, Radiology Center, University of Giessen, Klinikstrasse 36, Giessen 35385, Germany. Address correspondence to H. Gufler (h.gufler@ccb.de). 2 Department of Pathology, University of Giessen, Giessen, Germany. WEB This is a Web exclusive article. AJR 2007; 188:W480 W X/07/1885 W480 American Roentgen Ray Society High-Resolution MRI of Basal Cell Carcinomas of the Face Using a Microscopy Coil OBJECTIVE. The objective of this article is to evaluate the diagnostic accuracy of highresolution MRI using a microscopy surface coil to stage basal cell carcinomas of the face. CONCLUSION. High-resolution MRI using a microscopy surface coil is a promising method to determine the extension of basaliomas of the facial region and to exclude infiltration of bone by the tumor. oninvasive imaging and characterization of skin abnormalities N are of great interest in dermatology. MRI is an established method for this purpose when low-noise coils with minimized volume and customized imaging sequences are applied to optimize the signal-to-noise ratio (SNR) [1]. Thin and contiguous slices are needed for adequate MRI of the skin to differentiate between the dermal and subcutaneous layers [2 4]. Therefore, high-resolution MRI is essential to discriminate normal from abnormal features of the skin. Recent developments in MR technology allow the use of a combination of a microscopy surface coil with a small field of view and a high-field clinical 1.5-T system with customized pulse sequences, which together provide high-resolution images of the skin. The purpose of this prospective study was to compare high-resolution MR images of basal cell carcinomas (basaliomas) of the face with the results of histology. Subjects and Methods Seven patients with basaliomas of the face were examined between March 2003 and January The patients were two women 54 and 85 years old and five men who ranged in age between 51 and 89 years. MRI of each patient was performed with a 1.5-T system (Gyroscan Intera, Philips Medical Systems) with high-power gradients (amplitude, 60 mt; slew rate, 150 mt/m/s). We used a microscopy coil with a diameter of 47 mm that was fixed by straps so that the region examined and the radiofrequency coil were rigidly locked together to prevent motion artifacts. The MRI protocol included axial T1-weighted (TR/TE, 450/24; field of view, 60 mm; matrix, ; turbo factor, 3; voxel size, mm; excitations averaged, 3; acquisition time, 5.3 minutes) and T2-weighted turbo spin-echo (TSE) (TR range /TE eff, 3,000 4,500/100; turbo factor, 13; field of view, 60 mm; matrix size, ; voxel size, mm; excitations averaged, 3; acquisition time, 3.3 minutes) images. Optionally, T1-weighted sagittal or coronal images were also acquired. After the administration of gadopentetate dimeglumine, axial, sagittal, and coronal T1-weighted sequences with or without fat suppression were performed. The MRI studies were evaluated prospectively by two radiologists in consensus who assessed the extension of the tumor and decided whether there was involvement of the bone, nasal cartilage, subcutaneous tissue, or muscles. Signal intensities were measured in operator-defined regions of interest that contained at least 50 pixels. Regions of interest were drawn on the tumor, subcutaneous fat, dermal layer, bone, cartilage, and muscle, and SNRs were calculated. These measurements were performed as close to the tumor as possible because the signal intensities of the tissue diminished toward the borders of the field of view. The radiologists had no knowledge of the results of other imaging methods such as sonography or CT, and because the evaluation was performed preoperatively, they had no information about the histologic results. In a final step, the radiologic findings were correlated with the histologic results. Results The tumors were localized in the nasolabial fold (n = 4), cheek (n = 1), temporal region (n = 1), and infraorbital region (n =1). In one of the seven patients, MR examination was normal without evidence of a recurrent W480 AJR:188, May 2007

2 MRI of Basal Cell Carcinomas of the Face A C B D Fig year-old man with basal cell carcinoma of left temporal region. A, Axial T1-weighted unenhanced turbo spin-echo (TSE) image shows superficially ulcerated tumor penetrating superficial layer of fascia temporalis (arrow). B, Axial T1-weighted contrast-enhanced TSE image shows tumor enhances inhomogeneously. C, Coronal T1-weighted image shows that tumor reaches zygomatic bone (arrowheads), but there is uncertainty whether there is infiltration of bone. D, Coronal fat-suppressed T1-weighted image shows infiltration of zygomatic bone can be excluded. This finding was confirmed by histology. tumor. All patients were operated on after MRI had been performed. Four of the seven patients underwent MRI because recurrence of a basal cell carcinoma was suspected. The tumors were slightly hyperintense on the T1-weighted images (SNR, 23.8 ± 10.3 [SD]) compared with the muscle tissue (SNR, 13.3 ± 5.1) and isointense compared with the skin (SNR, 21.3 ± 3.6). In the T2-weighted im- AJR:188, May 2007 ages, the lesions were markedly hyperintense (SNR, 21.3 ± 13.5) compared with the muscle (SNR, 7.4 ± 2.8) and moderately hyperintense compared with the skin (SNR, 13.0 ± 4.3). Subjectively, unenhanced T1-weighted images seemed to be more useful than T2-weighted images in delineating the contour of the masses and in providing a higher signal contrast between the tumor and the surrounding tissues. Calculations of the tumor-to-tissue ratio showed that T2-weighted images are obviously more helpful in distinguishing the tumor from the normal skin, but T1-weighted images yielded higher contrast between the tumor and the subcutaneous fat. Signal enhancement of the tumor was calculated in four patients for whom contrast-enhanced T1-weighted TSE sequences without fat suppression were available. The increase in signal intensity after administration of contrast material ranged between 58% and 99% compared with unenhanced images. The normal skin enhanced within a wider range, between 10% and 74%. Involvement of the bone by the tumor could be excluded reliably in three patients by using T1weighted fat-suppressed contrast-enhanced sequences (Fig. 1). The size of the basaliomas ranged between 6.2 and 32.0 mm (mean, 15.9 mm). The extensions and the volumes of the tumors measured on MRI correlated highly with those measured on histology (R2 = 0.98 and R2 = 0.98, respectively). On MRI, periosteal infiltration was seen in one patient, and infiltration of muscle in four patients. These findings were confirmed by histology. A beginning infiltration of the tumor into the nasal cartilage could not be ruled out on the unenhanced MR images in one patient. On the contrast-enhanced images, however, this finding could not be corroborated. The histologic examination showed that there was a 2-mm gap between the tumor and the nasal cartilage, without any sign of tumorous infiltration (Fig. 2). Discussion A basal cell carcinoma (basalioma) is a semimalignant tumor of the skin that derives from incompletely differentiated immature keratinocytes of the epidermis or appendages of the skin [5]. The natural history of this tumor is characterized by a slow local infiltration with invasion and destruction of the underlying structures. Metastases of the tumor are extraordinarily rare. Basal cell carcinomas develop most likely on sun-exposed body sites. Areas of predilection on the face are the nose, cheeks, and nasolabial folds. On clinical examination, a basal cell carcinoma is a nodule with telangiectases and multiple small satellite nodules. The tumor may be pigmented, sclerotic (basalioma cicatricans), or ulcerated (ulcus rodens), and it may infiltrate deeper structures such as bone or cartilage (ulcus terebrans). Basal cell carcinomas are prone to recurrence. Especially in the case of a recurrent tumor, it is difficult to estimate the depth of infiltration W481

3 A B C Fig year-old man with recurrence of basal cell carcinoma of left nasal region. A, Axial T1-weighted turbo spin-echo image shows tumor that extends into depth of skin. Thin layer of fatty tissue separates tumor from nasal cartilage. Interruption of continuity of this layer (arrows) suggests tumor infiltration of nasal cartilage. B, Axial T1-weighted contrast-enhanced fat-suppressed image does not corroborate finding in A. There is no interruption of small layer of fat between tumor and cartilage (arrow). C, Photomicrograph of stained specimen shows tumor (T) does not reach nasal cartilage (C). (H and E) TABLE 1: Signal-to-Noise Ratio by Technique Technique Value Tumor Fat Muscle Skin Bone T1-weighted Mean SD p < < 0.06 < 0.60 < 0.04 T2-weighted Mean SD p < 0.09 < 0.02 < < T1-weighted, contrast-enhanced Mean SD p < 0.68 < 0.87 < 0.84 < Note Values for p calculated using Student s t test, with p < 0.05 signifying statistical significance (values in bold) between signal-to-noise ratio of tumor versus other tissue components. clinically and determine if bone, cartilage, muscles, or vessels are involved. Such cases require an imaging method that is able to discriminate the superficial structures from the deeper structures of the skin. Many studies have shown that MRI is a useful imaging tool to diagnose skin abnormalities [6 8]. Krug et al. [9] found that high-resolution MRI on a 1.5-T system allows identification of the main histologic patterns of inflammatory skin diseases noninvasively. However, the structures of the epidermis could not be assessed adequately due to limitations in spatial and contrast resolution. At 3 T, improved SNR and higher spatial resolution of human nerves were achieved [10]. Ashman et al. [11] showed a marked increase in SNR with 8 T. There is, however, an increase in magnetic susceptibility and chemical shift artifacts at higher field strengths [12, 13]. Magnetic susceptibility artifacts are known to be most prominent at the bone-to-air and bone-to-softtissue interfaces. Magnetic susceptibility increases if gradient-recalled echo sequences are used. Although a better SNR is achieved at high magnetic field strengths, Hawnaur et al. [14] reported that even at 0.5 T, the MRI findings correlated well with histologic findings in patients with skin tumors. The main purpose of this study was to produce high-quality, high-resolution images of basal cell carcinomas on a clinical 1.5-T system by means of a microscopy coil. High-resolution images with 2D TSE sequences were obtained by selecting 1.5-mm-thin slices, a 60-mm field of view, and an imaging matrix of mm (in-plane resolution, mm) for the T1-weighted and T2-weighted images. On a subjective visual basis, the margins of the tumor could be differentiated best from the surrounding tissue on the unenhanced T1-weighted spinecho images. However, measurements of signal intensity ratios between tumor and surrounding tissues showed that T1-weighted and T2- weighted TSE images were almost equivalent in the differences in contrast between tumor and bone and tumor and muscle. T1-weighted images yielded a higher contrast between tumor and fat; T2-weighted images had a superior contrast between tumor and normal skin (Table 1). Fat-suppressed contrast-enhanced T1-weighted images were essential to assess the infiltration of the bone. An incipient involvement of the nasal cartilage by the tumor could not be ruled out consistently in all sequences in one case. The histologic examination, however, showed no infiltration of the cartilage. The lesion of one patient with suspicion of a recurrent tumor on clinical and MR examination proved to be scar tissue with acute and chronic inflammation on histology (Fig. 3). The marked signal enhancement of the superficial layer of the scar with acute and chronic inflammation on histology after the administration of the contrast agent made the lesion indistinguishable from a recurrent tumor on MRI. Dynamic contrast-enhanced scans might have helped to differentiate scar tissue from tumor. W482 AJR:188, May 2007

4 MRI of Basal Cell Carcinomas of the Face A B Fig year-old man with suspicion of recurrent basal cell carcinoma of left nasal region. A, Axial T2-weighted turbo spin-echo image shows scar tissue in left nasolabial fold with extension to muscle layer. Surface is excavated, mimicking ulcerated recurrence of tumor (white arrow). MS = maxillary sinus. Black arrow = scar tissue. Star = mimic muscle. B, Axial T1-weighted contrast-enhanced fatsuppressed image shows enhancement of superficial region of scar (arrowheads) and lack of enhancement of deeper scar tissue. Histology revealed acute and chronic inflammation of superficial scar layer and no recurrence of basal cell carcinoma. A B C Fig year-old woman with nodule on left cheek. A, Axial T1-weighted unenhanced image shows small flat tumor nodule with central erosion (white arrow). Black arrow indicates mimic muscle. B, Axial T1-weighted contrast-enhanced image shows moderate enhancement of tumor (box). C, Photomicrograph of stained specimen shows close concordance with MR microscopy imaging. Solid arrows = tumor borders, open arrow = ulcerated tumor surface, V = vessels. (H and E) Our examination influenced the planning of the operation in the three patients with clinical suspicion of bone involvement that could be excluded by MRI. A recurrent tumor was definitively excluded by MRI in one case; however, an open biopsy was performed, confirming the diagnosis. A limitation of the 47-mm microscopy coil is that the signal intensity decreases markedly from the center to the periphery of the 6-cm field of view, so the determination of signal intensities represents a problem if the tumor is not in the center of the field of view. Another limitation with using microscopy coils is that the contralateral regions of the face are not available for comparison. Therefore, it may be difficult to detect superficially growing basaliomas. This shortcoming, however, could be avoided by using multichannel, multicoil imaging. A further limitation of this study is that 3D gradient-echo sequences were not used, which might have yielded even better results regarding spatial resolution and SNR. Song et al. [15] produced high-resolution images of the dermis by means of a customized 3D gradient, partial flip-angle spinecho pulse sequences, and very small transmit receive coils on a 1.5-T clinical scanner in vivo, obtaining voxel sizes as small as μm. We preferred spin-echo sequences to gradient-echo sequences to avoid susceptibility artifacts because many of the tumors were located near the nasal cavity or the maxillary sinus. Furthermore, there are only a small number of pulse sequences commercially available for microscopy coils. In conclusion, high-resolution MRI with a commercially available microscopy surface coil and a clinical high-field 1.5-T MR system with strong gradients is a suitable method to determine the extension and depth of infiltration of basal cell carcinomas of the facial region (Fig. 4). In the future, the diagnostic accuracy of high-resolution MRI of these tumors will improve with the use of 3-T MR systems and their combination with dedicated sequences and the microscopy coil. References 1. Liffers A, Vogt M, Ermert H. In vivo biomicroscopy of the skin with high-resolution magnetic resonance imaging and high frequency ultrasound. Biomed Tech 2003; 48: AJR:188, May 2007 W483

5 2. Mäurer J, Knollmann FD, Schlums D, et al. Role of high-resolution magnetic resonance imaging for differentiating melanin-containing skin tumors. Invest Radiol 1995; 11: Bittoun J, Saint-Jalmes H, Querleux BG, et al. In vivo high-resolution MR imaging of the skin in a wholebody system at 1.5 T. Radiology 1990; 176: Thali MJ, Dirnhofer R, Becker R, Oliver W, Potter K. Is virtual histology the next step after the virtual autopsy? Magnetic resonance microscopy in forensic medicine. Magn Reson Imaging 2004; 22: Schwartz RA. Skin cancer: recognition and management. New York, NY: Springer-Verlag, 1988: Mirrashed F, Sharp JC. In vivo morphological characterisation of skin by MRI micro-imaging methods. Skin Res Technol 2004; 10: Mirrashed F, Sharp JC, Krause V, Morgan J, Tomanek B. Pilot study of dermal and subcutaneous fat structures by MRI in individuals who differ in gender, BMI, and cellulite grading. Skin Res Technol 2004; 10: Pennasilico GM, Arcuri PP, Laschena F, et al. Magnetic resonance imaging in the diagnosis of melanoma: in vivo preliminary studies with dynamic contrast-enhanced subtraction. Melanoma Res 2002; 12: Krug B, Schulze HJ, Kugel H, Krahe T, Wesselmann C, Lackner K. Correlation of MRI and histopathological findings in inflammatory skin diseases [in German]. Rofo 1998; 168: Hormann M, Traxler H, Ba-Ssalamah A, et al. Correlative high-resolution MR-anatomic study of sciatic, ulnar and proper palmar digital nerve. Magn Reson Imaging 2003; 21: Ashman CJ, Farooki S, Abduljalil AM, Chakeres DW. In vivo high-resolution coronal MRI of the wrist at 8T. J Comput Assist Tomogr 2002; 26: Constable RT, Henkelman RM. Contrast, resolution, and detectability in MR imaging. J Comput Assist Tomogr 1991; 15: Abduljalil AM, Robitaille P-ML. Macroscopic susceptibility in ultra high field MRI. J Comput Assist Tomogr 1999; 23: Hawnaur JM, Dobson MJ, Zhu XP, Watson Y. Skin: MR imaging findings at middle field strength. Radiology 1996; 201: Song HK, Wehrli FW, Ma J. In vivo MR microscopy of the human skin. Magn Reson Med 1997; 37: W484 AJR:188, May 2007