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Value of MR and CT Imaging for Assessment of Internal Carotid Artery Encasement in Head and Neck Squamous Cell Carcinoma

Value of MR and CT Imaging for Assessment of Internal Carotid Artery Encasement in Head and Neck... Hindawi Publishing Corporation International Journal of Surgical Oncology Volume 2013, Article ID 968758, 6 pages http://dx.doi.org/10.1155/2013/968758 Clinical Study Value of MR and CT Imaging for Assessment of Internal Carotid Artery Encasement in Head and Neck Squamous Cell Carcinoma 1,2 3 3 4 W. L. Lodder, C. A. H. Lange, H. J. Teertstra, F. A. Pameijer, 1,5,6 1,5 M. W. M. van den Brekel, andA.J.M.Balm Department of Head & Neck Oncology and Surgery, The Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, Amsterdam, eTh Netherlands Department of Otorhinolaryngology/Head and Neck Surgery, eTh University Medical Center Groningen, University of Groningen, 9700 RB Groningen, eTh Netherlands Department of Radiology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands Department of Radiology, University Medical Centre Utrecht, Utrecht, eTh Netherlands Department of Otorhinolaryngology, Academic Medical Centre, University of Amsterdam, Amsterdam, eTh Netherlands InstituteofPhoneticSciences, ACLC,UniversityofAmsterdam,Amsterdam,TheNetherlands Correspondence should be addressed to W. L. Lodder; w.l.lodder@gmail.com Received 25 November 2012; Accepted 4 January 2013 Academic Editor: Masaki Mori Copyright © 2013 W. L. Lodder et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Objective. This study was conducted to assess the value of CT and MR imaging in the preoperative evaluation of ICA encasement. Methods. Based upon three patient groups this study was performed. Retrospective analysis of 260 neck dissection reports from 2001 to 2010 was performed to determine unexpected peroperative-diagnosed encasement. Two experienced head and neck radiologists reviewed 12 scans for encasement. Results. In four out of 260 (1.5%) patients undergoing neck dissection, preoperative imaging was false negative as there was peroperative encasement of the ICA. Of 380 patients undergoing preoperative imaging, the radiologist reported encasement of the ICA in 25 cases. In 342 cases no encasement was described, 125 of these underwent neck dissection, and 2 had encasement peroperatively. eTh interobserver variation kappa varied from 0.273 to 1 for the different characteristics studied. Conclusion. es Th e retrospectively studied cohorts demonstrate that preoperative assessment of encasement of the ICA using MRI and/or CT was of value in evaluation of ICA encasement and therefore contributively in selecting operable patients (without ICA encasement), since in only 1.5% encasement was missed. However, observer variation aec ff ts the reliability of this feature. 1. Introduction artery, as generally performed in vascular disease and glomus tumors, is possible, it is generally not advocated because the Preoperative diagnosis of internal carotid artery (ICA) outcome in oncologic patients is dismal [4]. involvement changes the primary treatment of head and neck Many attempts have been undertaken to classify carotid invasion on preoperative imaging including ultrasound, fol- tumors. Literature data on carotid encasement in head and neck cancer are scarce. One series reported on a 5% to 10% lowed by magnetic resonance imaging (MRI) and computed incidence of cervical lymph node metastases invading the tomography (CT) scan [1, 2, 5–13]. ICA not diagnosed on preoperative imaging using 5 different In 1995 Yousem et al. [2] demonstrated in a series of imaging signs [1]. Encasement of the ICA is both a poor 49 patients undergoing neck dissection for head and neck prognostic indicator and oen ft a contraindication to surgical tumors clinically suspicious for encasement that more than treatment [2]. Removal of lymph node metastases from the 270 degrees of circumferential involvement of the ICA on ICA may lead to stroke and carotid rupture in 3.3% and 5.5%, MRI predicted unresectable disease. eTh y reached sensitivity and specificity of 100% and 88%. Assessment of carotid respectively [3]. The risk for cerebral damage aeft r removal of the ICA is 3.3% to 30% [1]. Although grafting of the carotid invasion by ultrasonography had sensitivity up to 100% 2 International Journal of Surgical Oncology [10–13]. However, in this study we focused on the value of MR as positive sign for encasement. However, it was unclear and CT imaging. whether all radiologists used standardized criteria. Until now, no consensus has been reached on standard- (3) Evaluation of Radiologically Determined Criteria. Twelve ization of imaging criteria for defining encasement of the patients with peroperative encasement or preoperative carotid artery. MRI seems to be the most sensitive imaging encasement or possible encasement of the ICA were selected modality to visualize contrasts between soft tissues structures from the previously claimed cohorts. eTh ir pretreatment and therefore should be optimal for the assessment of carotid MRIs (𝑛=6 )and CTs(𝑛=6 )werereviewedamong 42 encasement. Apart from the publications of Pons et al. [1] other scans (with no ICA encasement) by two experienced and Yousem et al. [2], no other studies were performed head and neck radiologists (JT and CL) using criteria selected for classifying carotid encasement on MR imaging. Carotid from the literature [1, 2]. The observers were unaware of the encasement has a low incidence, but a high impact on peroperative n fi dings, of all 54 scans. eTh results of only the treatment planning. This study was conducted to assess the 12 with ICA involvement were used for assessment of the value of CT and MR imaging in the preoperative evalu- interobserver variation. ation of ICA encasement. er Th efore we studied 3 patient groups/cohorts retrospectively to review the number of cases with peroperative encasement of the ICA in our institution 2.2. MR Technique. For this study both MRI examinations (group 1) and to assess the prevalence of preoperatively were performed at 1,5 T. (Magnetom; Siemens Medical Sys- diagnosed encasement of the ICA on CT and MR scans tems, Erlangen, Germany) and 3.0 T. (Philips Achieva release (group 2) and interobserver variation (group 3). 3.2.1, Philips Medical Systems, Best, The Netherlands) using a dedicated 16-channel SENSE neurovascular coil. eTh fol- lowing series were acquired: STIR TSE COR, TR (repetition 2. Materials and Methods time), IR (inversion time), TE (echo time) 3,880/180/20 ms, ETL: 12, FOV 300/228/40 mm, matrix: 320/320, 2 nex, slice 2.1. Ethical Considerations. Institutional approval for the thickness 4 mm; STIR TSE TRA, TR/IR/TE 4,228/180/20, study was received. As patient anonymity was preserved ETL: 12, FOV: 180/200/80 mm, matrix 300/312, 2 nex, patient consent was not required for the retrospective review SW 3.5 mm, T1 TSE TRA, TR/TE: 780/10, ETL: 5, FOV of records and images. 180/180/80, matrix 384/384, 2 nex, slice thickness: 3.5 mm; eTh results of this study will be presented based upon following three dieff rent patient groups. T1 3D Thrive (performed aeft r intravenous injection of 15 cc gadoterate meglumine (Dotarem)), TR/TE: 5/2,22, ETL: 90, (1) Peroperative Assessment of Encasement of the ICA. Between TA: 10, FOV 230/272/220, matrix 288/288, 2 nex, slice thick- 2001 and 2011 a total of 551 patients (608 neck dissections) ness: 0.8 mm; T1 TSE COR (postcontrast): TR/TE: 812/10, who had undergone neck dissection in our institution for ETL: 6, FOV: 180/150/96 mm, matrix: 320/320, 3 nex, slice head and neck squamous cell carcinoma following a pre- thickness 3.5 mm. surgical MRIorCTworkupwereselectedfromour operation The mean time between imaging and neck dissection was database.Inour center,patientswithatumorlocated above 12 days (range 1–48; SD 19). the level of the hyoid bone or with an unknown primary tumor are preferentially studied with MR imaging. Aeft r a 2.3. CT Technique. CT studies were performed with one of rfi st evaluation of the 608 operation reports, 348 patients were two multidetector scanners (Philips Gemini TF or Siemens excluded (incomplete data, pathological N0-stage, or patho- Sensation). Standard CT of the neck was performed, after logical N1-stage). Two hundred and sixty operation reports the injection of nonionic contrast material (Omnipaque were evaluated for the presence of peroperative carotid 300 mg/mL, GE Health Care, quantity in mL equal to body encasement (Figure 1). All patients received a (modified) weight in kilograms) with an injection rate of 4 mL/sec. radical neck dissection or salvage selective neck dissection or Acquisition of 1,5 or 2 mm slices started aer ft 55 seconds, superselective lymph node dissection aeft r chemoradiation and the images were reformatted into 3-mm-thick sections therapy and underwent preoperative evaluation with CT or in transverse and coronal directions. MR imaging. 2.4. Studied Radiological Criteria for ICA Encasement. (2) Preoperative Assessment of Encasement of the ICA. CT- Encasement of the ICA was assessed using the following and MR image reports from 2009 to 2010 (𝑛 = 1486 ) radiological criteria selected from the literature [1, 2]: were reviewed retrospectively for encasement of the ICA to estimate the prevalence of preoperatively diagnosed carotid (1) encasement of the artery: none, 180–270,>270 deg- encasement. After a rfi st evaluation of the reports, 1106 out of rees, the 1486 imaging reports were excluded (cases with no aber- rations on imaging or with benign lesions were excluded; see (2) obliteration of the fat between the lymph node/pri- Figure 2). Three hundred and eighty reports were evaluated mary tumor and the carotid artery, for the presence of preoperative carotid encasement. These (3) deformation of the carotid artery, reports were from different radiologists using nonspecified criteria. Most of the radiologists used the criterion of>270 (4) length of contact between the carotid artery and tu- degrees circumferential involvement of the carotid artery mor mass. International Journal of Surgical Oncology 3 2001–2010 Patients𝑁= 551 Excluded (𝑛= 348) 𝑁= 608 pN0: 205 Neck dissections pN1: 89 After exclusion Incomplete data: 54 total𝑁= 260 Peroperative No encasement Encasement of ECA Encasement of ICA 𝑁= 236 𝑁= 20 𝑁= 4 encasement Clinical fixation Ultrasound finding CT/MRI Yes: 1 Encasement not MRI: 2 Clinical findings No: 3 reported: 4 CT: 2 Figure 1: Neck dissectionsperformed between2001and 2010.ECA:externalcarotid artery.ICA:internalcarotid artery.This figureshows 551 patients in which 608 neck dissections were performed. In total 260 cases were studied aeft r exclusion. In 236 cases no encasement was found during operation. In 20 cases (7.7%) encasement of the external carotid artery was seen. In four cases encasement of the internal carotid artery was present (4/260 = 1.5%). Two cases had MRI and 2 had CT preoperatively. 2.5. Statistics. Logistic regression was used to determine all encasement. In 342 cases (90%) the radiologist reported no significant characteristics for carotid encasement on MRI. To encasement. One hundred and twenty-five of these patients measure the interobserver agreement, the kappa coefficient were operated; in two patients peroperative encasement of was used. This coefficient can vary between −1(complete the ICA was present (2/125 = 1.6%), which was not reported disagreement) and +1 (complete agreement). If this measure during preoperative imaging (see Figure 2). takes on the value zero (0), the observer agreement can be interpreted as being the result of mere chance. A value of 3.3. Evaluation of Radiologically Determined Criteria. Two more than 0.75 can be interpreted as good agreement among radiologists reviewed 12 preoperative images of patients observers. The overall kappa coefficient can be interpreted as with known peroperative ICA encasement using the above- a measure of agreement between the groups of observers. mentioned criteria (see Figure 3). Table 1 shows the percent- ages of the radiologically determined criteria per observer and the interobserver variation. Interobserver kappa values 3. Results were low with values from 0.273 (deformation of the carotid artery) to high with value of 1 (obliteration of fat planes) for 3.1. Peroperative Assessment of Encasement of the ICA. In the different parameters. 24 of 260 cases (9.2%) peroperative encasement of both the internal or external carotid artery was found: in total 1.5% (4/260) of the cases undergoing a neck dissection 4. Discussion had encasement of the ICA (see Figure 1). In one case of encasement of the ICA, clinical xfi ation of the tumor on 4.1. Synopsis of Key/New Findings. These retrospectively physical examination was mentioned. studied cohorts demonstrate that preoperative assessment of encasement of the ICA using MRI and/or CT was missed in only 1.5%. However the criteria used in the literature show a 3.2. Preoperative Assessment of Encasement of the ICA. A high interobserver variation. total of 380 image reports were studied for the presence of preoperatively reported ICA encasement. In twenty-five cases (6.6%) the radiologist reported encasement. None 4.2. Comparisons with Other Studies. In 2010 Pons et al. [1] of these patients were operated. In thirteen cases (3.4%) studied the relevance of vfi e different imaging parameters the radiologist reported possible encasement. Of these 13 for evaluating carotid artery invasion in 22 patients with patients, vfi e underwent surgery and none had peroperative peroperatively proven encasement of the ICA. Of these 4 International Journal of Surgical Oncology 2009-2010 Patients𝑁= 1007 Total 1486 CT: 501 Excluded (𝑛= 1106) MRI: 985 No aberrations: 1068 Benign tumors: 38 After exclusion 𝑁= 380 Conclusion on Encasement− Encasement+ Possible encasement imaging 𝑁= 25 𝑁= 13 𝑁= 342 Other: Other: Other: CCRT: 129 CCRT: 2 CCRT: 3 Surgery Surgery Surgery No Treatment No No RT: 2 RT: 10 RT: 44 Cx: 3 0 9 5 Cx: 1 2 125 34 Cx: 3 PDT: 1 PDT: 0 PDT: 7 Encasement Encasement Encasement Encasement Peroperative − + − encasement 0 5 2 123 Figure 2: Retrospective analysis of all MR and CT images from 2009 to 2 010. CCRT: concomitant chemoradiation therapy, RT: radiotherapy, Cx: chemotherapy, and PDT: photodynamic therapy. This figure shows 1486 MR and CT studies performed in 1007 patients between 2009 and 2010. In 1068 cases no aberrations were found, and in 38 cases there were only benign tumors. In 25 cases encasement (>270 degrees encasement) was present at preoperative assessment. In 13 cases the report was not conclusive, and in 342 cases no encasement was seen. During operation in 2/125 = 1.6% cases, encasement of the internal carotid artery was found. (a) (b) Figure 3: Examples of CT and MR images showing carotid encasement. (a) Axial CT image of a lymph node metastases (the mass is encircled by a white line) at the right side showing at least 270 degrees of encasement. eTh conu fl ent lymph node mass is invading into the skin. The right carotid artery (arrow) is covered by the lymph node mass. Note: the right internal jugular vein is not visible, possibly due to compression. Suggestive the high-density structure (white star) lateral to the right lamina of the cricoid is surgical clip from earlier operation. (b) Fat- suppressed T1 contrast-enhanced MR section showing lymph node metastases in the left neck. eTh left internal carotid artery (arrow) is covered anteriorly and laterally by nodal disease (the mass is encircled by a white line). The circumferential involvement is (just) over 180 degrees. International Journal of Surgical Oncology 5 Table 1: Radiologically determined criteria and interobserver fat interface in 17 patients. All CT scans demonstrated this kappa. feature; however 16/17 = 94% was false positive. Yu et al. [9]studied in 2003 thediagnosticvalue of Radiologically Observer 1 Observer 2 Interobserver CT imaging for the detection of carotid encasement. In determined criteria N =12 N =12 kappa 27 patients, involvement of the common carotid artery or Encasement 0.584 internal carotid artery (11 tumors) or the jugular vein (25 <180 degrees 2 (17%) 0 (0%) tumors) was studied. In 17 cases the tumors did not involve the cervical vessels. eTh compression and deformation, more 180–270 degrees 0 (0%) 4 (33%) than 180 degrees circumference, undefined carotid artery >270 degrees 10 (83%) 8 (67%) wall, and fat or fascial plane deletion between tumor and Obliteration of fat 1 carotid wall were studied. With specificity ranging from planes 47.4% to 100% and sensitivity ranging from 18.5% to 90.9% No 0 0 they emphasized that a combination of criteria should be Yes used. 12 (100%) 12 (100%) Our results seem to confirm the results from the above- Deformation of the mentioned studies. Overall, it can be questioned whether 0.273 carotid artery preoperative imaging assessment of carotid encasement for No 4 (33%) 2 (17%) treatment selection should be used at all with no specicfi criteria available. Yes 8 (67%) 10 (83%) The false negative rate of preoperative assessment of Length of contact 0.488 encasement of the ICA was 1.5% in our retrospective cohorts, carotid artery using the intraoperative findings as “gold standard” for 3.5 3.6 carotid encasement. If the radiologist reported>270 degrees Mean in cm (range: 1.0–5.0; (range: 1.6–6.1; of carotid encasement according to our current protocol, SD 1.3) SD 1.6) patients were not operated. For the calculation of observer variation we used a small selection of twelve patients. eTh interobserver kappa varied from 0.273 to 1.00 for the different radiologically determined characteristics. patients, preoperative CT and MR images were analyzed. Size of the adenopathy and intensity of the contact showed Various studies showed survival with carotid resection no correlation with peroperative ndin fi gs. However, imaging was less than 15 months [14, 15]. In a meta-analysis of Sny- characteristics such as carotid artery deformation, encase- derman and D’Amico [16], 2-year disease-free survival was ment of >180 degrees, and segmental obliteration of the 22% aeft r carotid resection. With these low survival figures fat were significantly associated ( 𝑃 < 0.05 )withmassive in mind, one may seriously doubt whether carotid resection invasion of the carotid artery. In 1995 Yousem et al. [2]studied should be part of a standard surgical approach. MR images of 53 carotid arteries in 49 patients. Twenty-two MR images had a tumor surrounding the carotid artery less 4.3. Clinical Applicability of the Study. The importance of than 180 degrees and none of these had carotid artery invasion carotid artery encasement as a separate prognostic indicator at surgery. Seventeen arteries had more than 270 degrees of justifying an aggressive surgical approach with a high risk tumor encasement and twelve of these had invasion during of neurological complications can only be determined by a surgery (12/17 = 71%). Fourteen arteries had tumor with prospective multivariate analysis using standardized imaging 180–270 degrees of encasement on the preoperative imaging, techniques and agreement on radiological criteria. In daily with none having invasion at surgery. When the criterion of practice we still have to rely on the limitations of preoperative >270 degrees encasement was used, sensitivity of MRI was imaging. Most probably the combination of head and neck 100% and specificity 88%. In our series however, the criterion surgical and radiological expertise remains of crucial impor- of 270 degrees resulted in an interobserver kappa value tancetoassessthe resectabilityofnecknodemetastasesinan of 0.584. individual patient. Five articles reported on the value of preoperative CT Future research eor ff ts should be directed at more imaging. Sarvanan et al. [5] studied 26 patients and compared detailed depiction of the carotid artery wall. Increased res- palpation, ultrasound, and CT imaging. On CT, they studied olution may give more insight in the amount of invasion of encasement of>270 degrees and loss of fat planes. Sensitivity malignant neck disease in the various layers of the wall of the reached 75% and specificity 100%. Solano et al. [ 6]studied carotid artery. Use of high-field strength (3T) and application loss of afat interfacebetween thecarotid andthe neck mass. of surface coils may achieve this goal. There were 11 false positive ndings fi and one true positive finding. Rapoport et al. [ 7] studied in 2008 interobserver agreement based on a simplified two-item classification (0– 5. Conclusion 50% and 51–100% involvement). The general kappa was 0.53. In our specific and selected series interobserver variation These retrospectively studied cohorts demonstrate that pre- for categorical encasement (<180 versus 180–270 versus>270 operative assessment of encasement of the ICA using MRI degrees) was 0.584. Rothstein et al. [8]alsostudied loss of and/or CT was of value in evaluation of ICA encasement 6 International Journal of Surgical Oncology and therefore contributively in selecting operable patients [10] G. A. W. Gooding, A. W. Langman, W. P. Dillon, and M. J. Kaplan, “Malignant carotid artery invasion: sonographic (without ICA encasement), since in only 1.5% encasement detection,” Radiology,vol.171,no. 2, pp.435–438,1989. was missed. However, observer variation aeff cts the reliability [11] N. Gritzmann, M. C. Grasl, M. Helmer, and E. Steiner, “Invasion of this feature. of the carotid artery and jugular vein by lymph node metastases: Most probably the combination of head and neck surgical detection with sonography,” American JournalofRoentgenology, and radiological expertise remains of crucial importance to vol. 154, no. 2, pp. 411–414, 1990. assess the resectability of neck node metastases in an individ- [12] A. W. Langman, M. J. Kaplan, W. P. Dillon, and G. A. W. ual patient. eTh importance of carotid artery encasement as Gooding, “Radiologic assessment of tumor and the carotid a separate prognostic indicator justifying an aggressive sur- artery: correlation of magnetic resonance imaging, ultrasound, gicalapproachwithahigh risk of neurological complications andcomputedtomographywithsurgicalfindings,” Head and can only be determined by a prospective multivariate analysis Neck,vol.11, no.5,pp. 443–449, 1989. using standardized imaging techniques and agreement on [13] G. A. W. Gooding, “Malignant carotid invasion: sonographic radiological criteria. diagnosis,” ORL, vol. 55, no. 5, pp. 263–272, 1993. [14] T. R. Kroeker and J. C. O’Brien, “Carotid resection and recon- Conflict of Interests struction associated with treatment of head and neck cancer,” Proceedings (Baylor University. Medical Center),vol.24, no.4, eTh authors declare that there is no conflict of interests. pp. 295–298, 2011. [15] J.L.Roh,M.RaKim, S. H. Choi et al., “Can patients with head and neck cancers invading carotid artery gain survival References benefit from surgery?” Acta Oto-Laryngologica,vol.128,no. 12, pp. 1370–1374, 2008. [1] Y. Pons,E.Ukkola-Pons,P.Clemen ´ t, J. Gauthier, and C. Conessa, “Relevance of 5 different imaging signs in the evalu- [16] C. H. Snyderman and F. D’Amico, “Outcome of carotid artery ation of carotid artery invasion by cervical lymphadenopathy resection for neoplastic disease: a meta-analysis,” American in head and neck squamous cell carcinoma,” Oral Surgery, Oral Journal of Otolaryngology,vol.13, no.6,pp. 373–380, 1992. Medicine, Oral Pathology, Oral Radiology and Endodontology, vol. 109, no.5,pp. 775–778, 2010. [2] D.M.Yousem, H. Hatabu,R.W.Hurst et al., “Carotid artery invasion by head and neck masses: prediction with MR imag- ing,” Radiology,vol.195,no. 3, pp.715–720,1995. [3] E.Ozer,A.Agrawal,H.G.Ozer,and D. E. Schuller,“eTh impact of surgery in the management of the head and neck carcinoma involving the carotid artery,” Laryngoscope,vol.118,no. 10,pp. 1771–1774, 2008. [4] Z.S.Nemeth, G. Y. Domotor, M. Talos,J.Barabas,M.Ujpal,and G. Y. Szabo, “Resection and replacement of the carotid artery in metastatic head and neck cancer: literature review and case report,” International Journal of Oral and Maxillofacial Surgery, pp.645–650,2003. [5] K. Sarvanan, J. Rajiv Bapuraj, S. C. Sharma, B. D. Radotra, N. Khandelwal, and S. Suri, “Computed tomography and ultra- sonographic evaluation of metastatic cervical lymph nodes with surgicoclinicopathologic correlation,” Journal of Laryngology and Otology,vol.116,no. 3, pp.194–199,2002. [6] J.Solano, V. Garrido,and M. Mart´ınez-Morillo, “Ultrasonogra- phy is more eeff ctive than computed tomography in excluding invasion of the carotid wall by cervical lymphadenopathies,” European Journal of Radiology, vol. 17, no. 3, pp. 191–194, 1993. [7] A. Rapoport, O. D. S. Tornin, I. M. Beserra, P. B. C. De Neto, and R. P. De Souza, “Assessment of carotid artery invasion by lymph node metastasis from squamous cell carcinoma of aero- digestive tract,” Brazilian Journal of Otorhinolaryngology,vol. 74,no. 1, pp.79–84,2008. [8] S. G. Rothstein, M. S. Persky, and S. Horii, “Evaluation of malignantinvasionofthe carotidarterybyCTscanand ultrasound,” Laryngoscope, vol. 98, no. 3, pp. 321–324, 1988. [9] Q. Yu, P. Wang, H. Shi, and J. Luo, “Carotid artery and jugular vein invasion of oral-maxillofacial and neck malignant tumors: diagnostic value of computed tomography,” Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics,vol. 96, no. 3, pp. 368–372, 2003. 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Value of MR and CT Imaging for Assessment of Internal Carotid Artery Encasement in Head and Neck Squamous Cell Carcinoma

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Copyright © 2013 W. L. Lodder et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Hindawi Publishing Corporation International Journal of Surgical Oncology Volume 2013, Article ID 968758, 6 pages http://dx.doi.org/10.1155/2013/968758 Clinical Study Value of MR and CT Imaging for Assessment of Internal Carotid Artery Encasement in Head and Neck Squamous Cell Carcinoma 1,2 3 3 4 W. L. Lodder, C. A. H. Lange, H. J. Teertstra, F. A. Pameijer, 1,5,6 1,5 M. W. M. van den Brekel, andA.J.M.Balm Department of Head & Neck Oncology and Surgery, The Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, Amsterdam, eTh Netherlands Department of Otorhinolaryngology/Head and Neck Surgery, eTh University Medical Center Groningen, University of Groningen, 9700 RB Groningen, eTh Netherlands Department of Radiology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands Department of Radiology, University Medical Centre Utrecht, Utrecht, eTh Netherlands Department of Otorhinolaryngology, Academic Medical Centre, University of Amsterdam, Amsterdam, eTh Netherlands InstituteofPhoneticSciences, ACLC,UniversityofAmsterdam,Amsterdam,TheNetherlands Correspondence should be addressed to W. L. Lodder; w.l.lodder@gmail.com Received 25 November 2012; Accepted 4 January 2013 Academic Editor: Masaki Mori Copyright © 2013 W. L. Lodder et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Objective. This study was conducted to assess the value of CT and MR imaging in the preoperative evaluation of ICA encasement. Methods. Based upon three patient groups this study was performed. Retrospective analysis of 260 neck dissection reports from 2001 to 2010 was performed to determine unexpected peroperative-diagnosed encasement. Two experienced head and neck radiologists reviewed 12 scans for encasement. Results. In four out of 260 (1.5%) patients undergoing neck dissection, preoperative imaging was false negative as there was peroperative encasement of the ICA. Of 380 patients undergoing preoperative imaging, the radiologist reported encasement of the ICA in 25 cases. In 342 cases no encasement was described, 125 of these underwent neck dissection, and 2 had encasement peroperatively. eTh interobserver variation kappa varied from 0.273 to 1 for the different characteristics studied. Conclusion. es Th e retrospectively studied cohorts demonstrate that preoperative assessment of encasement of the ICA using MRI and/or CT was of value in evaluation of ICA encasement and therefore contributively in selecting operable patients (without ICA encasement), since in only 1.5% encasement was missed. However, observer variation aec ff ts the reliability of this feature. 1. Introduction artery, as generally performed in vascular disease and glomus tumors, is possible, it is generally not advocated because the Preoperative diagnosis of internal carotid artery (ICA) outcome in oncologic patients is dismal [4]. involvement changes the primary treatment of head and neck Many attempts have been undertaken to classify carotid invasion on preoperative imaging including ultrasound, fol- tumors. Literature data on carotid encasement in head and neck cancer are scarce. One series reported on a 5% to 10% lowed by magnetic resonance imaging (MRI) and computed incidence of cervical lymph node metastases invading the tomography (CT) scan [1, 2, 5–13]. ICA not diagnosed on preoperative imaging using 5 different In 1995 Yousem et al. [2] demonstrated in a series of imaging signs [1]. Encasement of the ICA is both a poor 49 patients undergoing neck dissection for head and neck prognostic indicator and oen ft a contraindication to surgical tumors clinically suspicious for encasement that more than treatment [2]. Removal of lymph node metastases from the 270 degrees of circumferential involvement of the ICA on ICA may lead to stroke and carotid rupture in 3.3% and 5.5%, MRI predicted unresectable disease. eTh y reached sensitivity and specificity of 100% and 88%. Assessment of carotid respectively [3]. The risk for cerebral damage aeft r removal of the ICA is 3.3% to 30% [1]. Although grafting of the carotid invasion by ultrasonography had sensitivity up to 100% 2 International Journal of Surgical Oncology [10–13]. However, in this study we focused on the value of MR as positive sign for encasement. However, it was unclear and CT imaging. whether all radiologists used standardized criteria. Until now, no consensus has been reached on standard- (3) Evaluation of Radiologically Determined Criteria. Twelve ization of imaging criteria for defining encasement of the patients with peroperative encasement or preoperative carotid artery. MRI seems to be the most sensitive imaging encasement or possible encasement of the ICA were selected modality to visualize contrasts between soft tissues structures from the previously claimed cohorts. eTh ir pretreatment and therefore should be optimal for the assessment of carotid MRIs (𝑛=6 )and CTs(𝑛=6 )werereviewedamong 42 encasement. Apart from the publications of Pons et al. [1] other scans (with no ICA encasement) by two experienced and Yousem et al. [2], no other studies were performed head and neck radiologists (JT and CL) using criteria selected for classifying carotid encasement on MR imaging. Carotid from the literature [1, 2]. The observers were unaware of the encasement has a low incidence, but a high impact on peroperative n fi dings, of all 54 scans. eTh results of only the treatment planning. This study was conducted to assess the 12 with ICA involvement were used for assessment of the value of CT and MR imaging in the preoperative evalu- interobserver variation. ation of ICA encasement. er Th efore we studied 3 patient groups/cohorts retrospectively to review the number of cases with peroperative encasement of the ICA in our institution 2.2. MR Technique. For this study both MRI examinations (group 1) and to assess the prevalence of preoperatively were performed at 1,5 T. (Magnetom; Siemens Medical Sys- diagnosed encasement of the ICA on CT and MR scans tems, Erlangen, Germany) and 3.0 T. (Philips Achieva release (group 2) and interobserver variation (group 3). 3.2.1, Philips Medical Systems, Best, The Netherlands) using a dedicated 16-channel SENSE neurovascular coil. eTh fol- lowing series were acquired: STIR TSE COR, TR (repetition 2. Materials and Methods time), IR (inversion time), TE (echo time) 3,880/180/20 ms, ETL: 12, FOV 300/228/40 mm, matrix: 320/320, 2 nex, slice 2.1. Ethical Considerations. Institutional approval for the thickness 4 mm; STIR TSE TRA, TR/IR/TE 4,228/180/20, study was received. As patient anonymity was preserved ETL: 12, FOV: 180/200/80 mm, matrix 300/312, 2 nex, patient consent was not required for the retrospective review SW 3.5 mm, T1 TSE TRA, TR/TE: 780/10, ETL: 5, FOV of records and images. 180/180/80, matrix 384/384, 2 nex, slice thickness: 3.5 mm; eTh results of this study will be presented based upon following three dieff rent patient groups. T1 3D Thrive (performed aeft r intravenous injection of 15 cc gadoterate meglumine (Dotarem)), TR/TE: 5/2,22, ETL: 90, (1) Peroperative Assessment of Encasement of the ICA. Between TA: 10, FOV 230/272/220, matrix 288/288, 2 nex, slice thick- 2001 and 2011 a total of 551 patients (608 neck dissections) ness: 0.8 mm; T1 TSE COR (postcontrast): TR/TE: 812/10, who had undergone neck dissection in our institution for ETL: 6, FOV: 180/150/96 mm, matrix: 320/320, 3 nex, slice head and neck squamous cell carcinoma following a pre- thickness 3.5 mm. surgical MRIorCTworkupwereselectedfromour operation The mean time between imaging and neck dissection was database.Inour center,patientswithatumorlocated above 12 days (range 1–48; SD 19). the level of the hyoid bone or with an unknown primary tumor are preferentially studied with MR imaging. Aeft r a 2.3. CT Technique. CT studies were performed with one of rfi st evaluation of the 608 operation reports, 348 patients were two multidetector scanners (Philips Gemini TF or Siemens excluded (incomplete data, pathological N0-stage, or patho- Sensation). Standard CT of the neck was performed, after logical N1-stage). Two hundred and sixty operation reports the injection of nonionic contrast material (Omnipaque were evaluated for the presence of peroperative carotid 300 mg/mL, GE Health Care, quantity in mL equal to body encasement (Figure 1). All patients received a (modified) weight in kilograms) with an injection rate of 4 mL/sec. radical neck dissection or salvage selective neck dissection or Acquisition of 1,5 or 2 mm slices started aer ft 55 seconds, superselective lymph node dissection aeft r chemoradiation and the images were reformatted into 3-mm-thick sections therapy and underwent preoperative evaluation with CT or in transverse and coronal directions. MR imaging. 2.4. Studied Radiological Criteria for ICA Encasement. (2) Preoperative Assessment of Encasement of the ICA. CT- Encasement of the ICA was assessed using the following and MR image reports from 2009 to 2010 (𝑛 = 1486 ) radiological criteria selected from the literature [1, 2]: were reviewed retrospectively for encasement of the ICA to estimate the prevalence of preoperatively diagnosed carotid (1) encasement of the artery: none, 180–270,>270 deg- encasement. After a rfi st evaluation of the reports, 1106 out of rees, the 1486 imaging reports were excluded (cases with no aber- rations on imaging or with benign lesions were excluded; see (2) obliteration of the fat between the lymph node/pri- Figure 2). Three hundred and eighty reports were evaluated mary tumor and the carotid artery, for the presence of preoperative carotid encasement. These (3) deformation of the carotid artery, reports were from different radiologists using nonspecified criteria. Most of the radiologists used the criterion of>270 (4) length of contact between the carotid artery and tu- degrees circumferential involvement of the carotid artery mor mass. International Journal of Surgical Oncology 3 2001–2010 Patients𝑁= 551 Excluded (𝑛= 348) 𝑁= 608 pN0: 205 Neck dissections pN1: 89 After exclusion Incomplete data: 54 total𝑁= 260 Peroperative No encasement Encasement of ECA Encasement of ICA 𝑁= 236 𝑁= 20 𝑁= 4 encasement Clinical fixation Ultrasound finding CT/MRI Yes: 1 Encasement not MRI: 2 Clinical findings No: 3 reported: 4 CT: 2 Figure 1: Neck dissectionsperformed between2001and 2010.ECA:externalcarotid artery.ICA:internalcarotid artery.This figureshows 551 patients in which 608 neck dissections were performed. In total 260 cases were studied aeft r exclusion. In 236 cases no encasement was found during operation. In 20 cases (7.7%) encasement of the external carotid artery was seen. In four cases encasement of the internal carotid artery was present (4/260 = 1.5%). Two cases had MRI and 2 had CT preoperatively. 2.5. Statistics. Logistic regression was used to determine all encasement. In 342 cases (90%) the radiologist reported no significant characteristics for carotid encasement on MRI. To encasement. One hundred and twenty-five of these patients measure the interobserver agreement, the kappa coefficient were operated; in two patients peroperative encasement of was used. This coefficient can vary between −1(complete the ICA was present (2/125 = 1.6%), which was not reported disagreement) and +1 (complete agreement). If this measure during preoperative imaging (see Figure 2). takes on the value zero (0), the observer agreement can be interpreted as being the result of mere chance. A value of 3.3. Evaluation of Radiologically Determined Criteria. Two more than 0.75 can be interpreted as good agreement among radiologists reviewed 12 preoperative images of patients observers. The overall kappa coefficient can be interpreted as with known peroperative ICA encasement using the above- a measure of agreement between the groups of observers. mentioned criteria (see Figure 3). Table 1 shows the percent- ages of the radiologically determined criteria per observer and the interobserver variation. Interobserver kappa values 3. Results were low with values from 0.273 (deformation of the carotid artery) to high with value of 1 (obliteration of fat planes) for 3.1. Peroperative Assessment of Encasement of the ICA. In the different parameters. 24 of 260 cases (9.2%) peroperative encasement of both the internal or external carotid artery was found: in total 1.5% (4/260) of the cases undergoing a neck dissection 4. Discussion had encasement of the ICA (see Figure 1). In one case of encasement of the ICA, clinical xfi ation of the tumor on 4.1. Synopsis of Key/New Findings. These retrospectively physical examination was mentioned. studied cohorts demonstrate that preoperative assessment of encasement of the ICA using MRI and/or CT was missed in only 1.5%. However the criteria used in the literature show a 3.2. Preoperative Assessment of Encasement of the ICA. A high interobserver variation. total of 380 image reports were studied for the presence of preoperatively reported ICA encasement. In twenty-five cases (6.6%) the radiologist reported encasement. None 4.2. Comparisons with Other Studies. In 2010 Pons et al. [1] of these patients were operated. In thirteen cases (3.4%) studied the relevance of vfi e different imaging parameters the radiologist reported possible encasement. Of these 13 for evaluating carotid artery invasion in 22 patients with patients, vfi e underwent surgery and none had peroperative peroperatively proven encasement of the ICA. Of these 4 International Journal of Surgical Oncology 2009-2010 Patients𝑁= 1007 Total 1486 CT: 501 Excluded (𝑛= 1106) MRI: 985 No aberrations: 1068 Benign tumors: 38 After exclusion 𝑁= 380 Conclusion on Encasement− Encasement+ Possible encasement imaging 𝑁= 25 𝑁= 13 𝑁= 342 Other: Other: Other: CCRT: 129 CCRT: 2 CCRT: 3 Surgery Surgery Surgery No Treatment No No RT: 2 RT: 10 RT: 44 Cx: 3 0 9 5 Cx: 1 2 125 34 Cx: 3 PDT: 1 PDT: 0 PDT: 7 Encasement Encasement Encasement Encasement Peroperative − + − encasement 0 5 2 123 Figure 2: Retrospective analysis of all MR and CT images from 2009 to 2 010. CCRT: concomitant chemoradiation therapy, RT: radiotherapy, Cx: chemotherapy, and PDT: photodynamic therapy. This figure shows 1486 MR and CT studies performed in 1007 patients between 2009 and 2010. In 1068 cases no aberrations were found, and in 38 cases there were only benign tumors. In 25 cases encasement (>270 degrees encasement) was present at preoperative assessment. In 13 cases the report was not conclusive, and in 342 cases no encasement was seen. During operation in 2/125 = 1.6% cases, encasement of the internal carotid artery was found. (a) (b) Figure 3: Examples of CT and MR images showing carotid encasement. (a) Axial CT image of a lymph node metastases (the mass is encircled by a white line) at the right side showing at least 270 degrees of encasement. eTh conu fl ent lymph node mass is invading into the skin. The right carotid artery (arrow) is covered by the lymph node mass. Note: the right internal jugular vein is not visible, possibly due to compression. Suggestive the high-density structure (white star) lateral to the right lamina of the cricoid is surgical clip from earlier operation. (b) Fat- suppressed T1 contrast-enhanced MR section showing lymph node metastases in the left neck. eTh left internal carotid artery (arrow) is covered anteriorly and laterally by nodal disease (the mass is encircled by a white line). The circumferential involvement is (just) over 180 degrees. International Journal of Surgical Oncology 5 Table 1: Radiologically determined criteria and interobserver fat interface in 17 patients. All CT scans demonstrated this kappa. feature; however 16/17 = 94% was false positive. Yu et al. [9]studied in 2003 thediagnosticvalue of Radiologically Observer 1 Observer 2 Interobserver CT imaging for the detection of carotid encasement. In determined criteria N =12 N =12 kappa 27 patients, involvement of the common carotid artery or Encasement 0.584 internal carotid artery (11 tumors) or the jugular vein (25 <180 degrees 2 (17%) 0 (0%) tumors) was studied. In 17 cases the tumors did not involve the cervical vessels. eTh compression and deformation, more 180–270 degrees 0 (0%) 4 (33%) than 180 degrees circumference, undefined carotid artery >270 degrees 10 (83%) 8 (67%) wall, and fat or fascial plane deletion between tumor and Obliteration of fat 1 carotid wall were studied. With specificity ranging from planes 47.4% to 100% and sensitivity ranging from 18.5% to 90.9% No 0 0 they emphasized that a combination of criteria should be Yes used. 12 (100%) 12 (100%) Our results seem to confirm the results from the above- Deformation of the mentioned studies. Overall, it can be questioned whether 0.273 carotid artery preoperative imaging assessment of carotid encasement for No 4 (33%) 2 (17%) treatment selection should be used at all with no specicfi criteria available. Yes 8 (67%) 10 (83%) The false negative rate of preoperative assessment of Length of contact 0.488 encasement of the ICA was 1.5% in our retrospective cohorts, carotid artery using the intraoperative findings as “gold standard” for 3.5 3.6 carotid encasement. If the radiologist reported>270 degrees Mean in cm (range: 1.0–5.0; (range: 1.6–6.1; of carotid encasement according to our current protocol, SD 1.3) SD 1.6) patients were not operated. For the calculation of observer variation we used a small selection of twelve patients. eTh interobserver kappa varied from 0.273 to 1.00 for the different radiologically determined characteristics. patients, preoperative CT and MR images were analyzed. Size of the adenopathy and intensity of the contact showed Various studies showed survival with carotid resection no correlation with peroperative ndin fi gs. However, imaging was less than 15 months [14, 15]. In a meta-analysis of Sny- characteristics such as carotid artery deformation, encase- derman and D’Amico [16], 2-year disease-free survival was ment of >180 degrees, and segmental obliteration of the 22% aeft r carotid resection. With these low survival figures fat were significantly associated ( 𝑃 < 0.05 )withmassive in mind, one may seriously doubt whether carotid resection invasion of the carotid artery. In 1995 Yousem et al. [2]studied should be part of a standard surgical approach. MR images of 53 carotid arteries in 49 patients. Twenty-two MR images had a tumor surrounding the carotid artery less 4.3. Clinical Applicability of the Study. The importance of than 180 degrees and none of these had carotid artery invasion carotid artery encasement as a separate prognostic indicator at surgery. Seventeen arteries had more than 270 degrees of justifying an aggressive surgical approach with a high risk tumor encasement and twelve of these had invasion during of neurological complications can only be determined by a surgery (12/17 = 71%). Fourteen arteries had tumor with prospective multivariate analysis using standardized imaging 180–270 degrees of encasement on the preoperative imaging, techniques and agreement on radiological criteria. In daily with none having invasion at surgery. When the criterion of practice we still have to rely on the limitations of preoperative >270 degrees encasement was used, sensitivity of MRI was imaging. Most probably the combination of head and neck 100% and specificity 88%. In our series however, the criterion surgical and radiological expertise remains of crucial impor- of 270 degrees resulted in an interobserver kappa value tancetoassessthe resectabilityofnecknodemetastasesinan of 0.584. individual patient. Five articles reported on the value of preoperative CT Future research eor ff ts should be directed at more imaging. Sarvanan et al. [5] studied 26 patients and compared detailed depiction of the carotid artery wall. Increased res- palpation, ultrasound, and CT imaging. On CT, they studied olution may give more insight in the amount of invasion of encasement of>270 degrees and loss of fat planes. Sensitivity malignant neck disease in the various layers of the wall of the reached 75% and specificity 100%. Solano et al. [ 6]studied carotid artery. Use of high-field strength (3T) and application loss of afat interfacebetween thecarotid andthe neck mass. of surface coils may achieve this goal. There were 11 false positive ndings fi and one true positive finding. Rapoport et al. [ 7] studied in 2008 interobserver agreement based on a simplified two-item classification (0– 5. Conclusion 50% and 51–100% involvement). The general kappa was 0.53. In our specific and selected series interobserver variation These retrospectively studied cohorts demonstrate that pre- for categorical encasement (<180 versus 180–270 versus>270 operative assessment of encasement of the ICA using MRI degrees) was 0.584. Rothstein et al. [8]alsostudied loss of and/or CT was of value in evaluation of ICA encasement 6 International Journal of Surgical Oncology and therefore contributively in selecting operable patients [10] G. A. W. Gooding, A. W. Langman, W. P. Dillon, and M. J. Kaplan, “Malignant carotid artery invasion: sonographic (without ICA encasement), since in only 1.5% encasement detection,” Radiology,vol.171,no. 2, pp.435–438,1989. was missed. However, observer variation aeff cts the reliability [11] N. Gritzmann, M. C. Grasl, M. Helmer, and E. Steiner, “Invasion of this feature. of the carotid artery and jugular vein by lymph node metastases: Most probably the combination of head and neck surgical detection with sonography,” American JournalofRoentgenology, and radiological expertise remains of crucial importance to vol. 154, no. 2, pp. 411–414, 1990. assess the resectability of neck node metastases in an individ- [12] A. W. Langman, M. J. Kaplan, W. P. Dillon, and G. A. W. ual patient. eTh importance of carotid artery encasement as Gooding, “Radiologic assessment of tumor and the carotid a separate prognostic indicator justifying an aggressive sur- artery: correlation of magnetic resonance imaging, ultrasound, gicalapproachwithahigh risk of neurological complications andcomputedtomographywithsurgicalfindings,” Head and can only be determined by a prospective multivariate analysis Neck,vol.11, no.5,pp. 443–449, 1989. using standardized imaging techniques and agreement on [13] G. A. W. Gooding, “Malignant carotid invasion: sonographic radiological criteria. diagnosis,” ORL, vol. 55, no. 5, pp. 263–272, 1993. [14] T. R. Kroeker and J. C. O’Brien, “Carotid resection and recon- Conflict of Interests struction associated with treatment of head and neck cancer,” Proceedings (Baylor University. Medical Center),vol.24, no.4, eTh authors declare that there is no conflict of interests. pp. 295–298, 2011. [15] J.L.Roh,M.RaKim, S. H. 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Schuller,“eTh impact of surgery in the management of the head and neck carcinoma involving the carotid artery,” Laryngoscope,vol.118,no. 10,pp. 1771–1774, 2008. [4] Z.S.Nemeth, G. Y. Domotor, M. Talos,J.Barabas,M.Ujpal,and G. Y. Szabo, “Resection and replacement of the carotid artery in metastatic head and neck cancer: literature review and case report,” International Journal of Oral and Maxillofacial Surgery, pp.645–650,2003. [5] K. Sarvanan, J. Rajiv Bapuraj, S. C. Sharma, B. D. Radotra, N. Khandelwal, and S. Suri, “Computed tomography and ultra- sonographic evaluation of metastatic cervical lymph nodes with surgicoclinicopathologic correlation,” Journal of Laryngology and Otology,vol.116,no. 3, pp.194–199,2002. [6] J.Solano, V. Garrido,and M. Mart´ınez-Morillo, “Ultrasonogra- phy is more eeff ctive than computed tomography in excluding invasion of the carotid wall by cervical lymphadenopathies,” European Journal of Radiology, vol. 17, no. 3, pp. 191–194, 1993. [7] A. Rapoport, O. 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