Neuroradiolog y/Head and Neck Imaging • Original Research Fornage et al. Transoral Ultrasound of Retropharyngeal Masses
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Neuroradiology/Head and Neck Imaging Original Research
Use of Transoral Sonography With an Endocavitary Transducer in Diagnosis, Fine-Needle Aspiration Biopsy, and Intraoperative Localization of Retropharyngeal Masses Bruno D. Fornage1,2 Beth S. Edeiken1 Gary L. Clayman2 Fornage BD, Edeiken BS, Clayman GL
Keywords: fine-needle aspiration biopsy, retropharyngeal lymph node metastases, thyroid cancer, transoral, ultrasound DOI:10.2214/AJR.13.11398 Received June 17, 2013; accepted after revision September 23, 2013. 1 Department of Diagnostic Radiology, The University of Texas M. D. Anderson Cancer Center, Unit 1350, 1155 Pressler St, Houston, TX 77030-3721. Address correspondence to B. D. Fornage ([email protected]). 2 Department of Surgical Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX.
WEB This is a web exclusive article. Supplemental Data Available online at www.ajronline.org. AJR 2014; 202:W481–W486 0361–803X/14/2025–W481 © American Roentgen Ray Society
OBJECTIVE. The purpose of this article is to describe the use of transoral sonography in the diagnosis, fine-needle aspiration (FNA) biopsy, and intraoperative localization of retropharyngeal masses. MATERIALS AND METHODS. We reviewed images and data for eight patients with a retropharyngeal mass identified on CT, MRI, or PET/CT as being suspicious for a metastatic Rouviere node. Transoral ultrasound was performed using a commercially available endorectal or endovaginal transducer. Transoral ultrasound–guided FNA biopsy was performed using a needle guide attached to the transducer shaft. Color and power Doppler imaging were used to identify the internal carotid artery and jugular vein and to plan the safest path to the targeted mass. The mass was intraoperatively localized by marking the mucosa with a permanent marker or by injecting methylene blue. RESULTS. There were six patients with a history of thyroid cancer (five papillary cancers and one medullary cancer), one patient with a history of esthesioneuroblastoma, and one patient with no history of cancer. Transoral ultrasound imaging was successful in all eight patients. Transoral ultrasound–guided FNA biopsy was performed in four patients, and a satisfactory cytologic diagnosis was obtained in all cases, although in one of those four cases, an additional core biopsy with an 18-gauge needle was performed to completely rule out lymphoma. Six patients underwent a transoral resection of the lesion. In three of them, the lesion was localized intraoperatively by making a mark on the mucosa and in one case by adding transoral ultrasound–guided injection of methylene blue. CONCLUSION. Transoral ultrasound can be used to visualize, sample, and localize abnormal masses in the retropharyngeal space, such as metastatic Rouviere nodes in patients with a history of head and neck cancer.
T
he retropharyngeal space is a potential space limited by the buccopharyngeal fascia and pharyngeal constrictor muscles anteriorly and the alar layer of prevertebral fascia posteriorly. It communicates with the parapharyngeal space. A fibrous raphe divides it into two lateral compartments, each containing fibrofatty tissue and retropharyngeal nodes known as Rouviere nodes, which are located medially to the internal carotid artery. Rouviere nodes usually regress during early childhood, but they can be a site of metastatic disease in patients with certain head and neck cancers, especially thyroid cancer. When involved, these nodes are detected on CT, MRI, or PET/CT scans obtained during cancer follow-up or for other reasons [1–3].
Currently, when a mass is detected in the retropharyngeal space, a preoperative tissue diagnosis can be obtained only via a CT-guided biopsy with a difficult subzygomatic or retromaxillary approach [4]. Here, we describe the use of direct transoral ultrasound in the diagnosis, fine-needle aspiration (FNA) biopsy, and intraoperative localization of masses in the retropharyngeal space and report our preliminary findings in a series of eight patients. Materials and Methods This retrospective review included transoral ultrasound images and reports from eight patients in whom CT, MRI, or PET/CT had revealed a mass in the retropharyngeal space that had been initially identified as suspicious for a metastatic Rouviere node. The patients underwent transoral ultrasound–guided needle biopsy and/or minimally
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Fornage et al. invasive transoral resection. Three patients were included in two previous publications detailing the surgical technique of transoral resection [5, 6]. This review was approved by our institution’s institutional review board and was compliant with HIPAA regulations.
Transoral Ultrasound Examination of the Retropharyngeal Space The transoral ultrasound examination was performed in the operating room. All but one patient had been prepared for a possible transoral resection and were under general anesthesia; the remaining patient was examined under local anesthesia. The patient was intubated with an armored size 6 or 7 endotracheal tube that was retracted and stabilized with a standard McIvor type of oral retractor commonly used in tonsillar surgery. There was no interference between the endotracheal tube and the placement of the endocavitary probe (Fig. 1). We used an ultrasound scanner (Prosound α 10, Hitachi-Aloka) equipped with a 3.0- to-8.5-MHz endorectal probe (UST-675P, Hitachi-Aloka) in three patients and a 2.5- to-7.5-MHz endovaginal transducer (UST-9118, Hitachi-Aloka) in five patients. Both probes have an outer diameter of 2.3 cm at the tip (scan head) and offer an end-firing 180° FOV. In the first patient, an attempt had also been made to use an intraoperative 3.75- to-10.0-MHz curved-array small-footprint finger-grip probe (UST 9132I, Hitachi-Aloka) with a 70° scanning angle. After its last use, the transducer was sterilized by being immersed in a 0.55% solution of ortho-phthalaldehyde (Cidex OPA, Ethicon) for 15 minutes, followed by gas sterilization with hydrogen peroxide gas for 1 hour. The endocavitary probe was fitted with a dedicated probe cover (NeoGuard, Civco Medical Solutions) after a small amount of sterile coupling gel had been deposited on the scan head. No coupling gel was necessary on the outside of the covered probe because the normal secretions covering the pharyngeal mucosa were sufficient to obtain a satisfactory acoustic coupling and images of good quality. Gray-scale and color and power Doppler imaging were used in all examinations. On occasion, transducer compression was applied through the pharyngeal wall so that the deformability of the lesion could be appreciated. Orthogonal (usually longitudinal but sometimes sagittal oblique and transverse) sonograms were obtained of each lesion. All lesions were measured, and their echogenicity and echotexture were evaluated, especially for the presence of cystic areas and microcalcifications. Color and power Doppler imaging were used to identify the internal carotid artery (ICA) and internal jugular vein (IJV) and to evaluate lesions’ internal vascularity after optimizing the color Doppler settings (mostly the pulse repetition frequency) of the scanner.
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Fig. 1—Intraoperative setting. Photograph shows that oral retractor is in place, and soft palate has been retracted with soft rubber catheter. Endocavitary probe has been inserted in oral cavity.
Ultrasound-Guided FNA Biopsy of Retropharyngeal Space Masses A metallic needle guide (MP-2748 for the UST9118 endovaginal probe or MP-2452 for the UST675P endorectal probe, all from Hitachi-Aloka) was attached securely along the shaft of the endocavitary probe (Fig. 2). The guide has been designed so that the needle is completely included in the sector scan plane after it exits the guide. A 25cm 20-gauge needle was used to accommodate the length of the needle guide. The probe equipped with the needle guide was inserted in the oral cavity, and its extremity was placed in direct contact with the pharyngeal mucosa. A gray-scale sonogram of the retropharyngeal space appeared on the monitor. Color or power Doppler ultrasound was used to identify the ICA and IJV. A built-in electronic biopsy line was activated and superimposed on the gray-scale sonogram to indicate the expected trajectory of the needle. The position of the transducer was adjusted so that the biopsy line would cross the suspicious mass. The needle was then inserted through the guide. Mild resistance was felt as the needle tip came into contact with the pharyngeal wall. Although the 20-gauge needle has a sharp bevel, a short thrust was often needed to pierce the wall. The needle then entered the sector FOV and appeared as a brightly echogenic line (see Video S1, which can be viewed by clicking Supplemental at the top of this article and then clicking the video number on the Supplemental page). The clear visualization of the needle tip allowed the operator to keep it within the limits of the target lesion during the FNA biopsy and at a safe distance from the ICA and IJV. Cellular material was aspirated from the retropharyngeal space mass by applying moderate (1–2 mL) but continuous negative pressure using the hand holding the syringe while holding the transducer in place with the other hand. The aspiration process lasted about 20–30 seconds, during which the needle was moved to and fro to mechanically
tear off and aspirate sheaths of cells from the lesion and to increase the volume of the aspirate. Because of the length of the needle, the appearance of blood-tinged material in the hub guaranteed that the aspirated material was quantitatively adequate because the whole length of the needle would be filled with cellular material. Aspiration was then stopped, and after the suction had been released, the needle-syringe assembly was pulled out of the needle guide. The cellular aspirate was recovered from the needle and smeared on a few slides. All smears were prepared by the radiologist; the slides were fixed and sent to the cytopathology laboratory, where they were stained using a Romanowsky stain (DiffQuick, Fisher Scientific) technique. A cytopathologist was available to provide a preliminary diagnosis within 15 minutes. In one case, the transoral ultra-
Fig. 2—Photograph shows endocavitary probe equipped with needle guide for needle biopsy. Dotted line indicates trajectory of needle.
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Transoral Ultrasound of Retropharyngeal Masses
A
B Fig. 3—59-year-old woman with history of papillary thyroid cancer and metastatic Rouviere node. A, Transverse gray-scale sonogram of left retropharyngeal space shows enlarged node with internal cystic areas (arrows) adjacent to internal carotid artery (ICA). B, Longitudinal sonogram shows node in its longest axis and shows cluster of microcalcifications (arrow) in addition to cystic areas. C, Power Doppler sonogram shows ICA adjacent to node. Note increased vascularity in metastatic node.
C sound–guided FNA biopsy was followed by a core needle biopsy, performed using the same type of transoral ultrasound guidance and an 18-gauge disposable automated biopsy device (Maxcore, Bard). The final diagnosis of malignancy was based on the cytopathological diagnosis. Clinical or imaging follow-up data were obtained for the patients with a benign cytopathological diagnosis.
Intraoperative Localization of Lesions Before Transoral Resection In selected cases, the retropharyngeal space mass was localized intraoperatively with transoral ultrasound before transoral resection using a simple marking of the lesion projection on the pharyngeal mucosa with a permanent marker or the injection of a small amount (< 1 mL) of methylene blue into the perilesional tissues according to the surgeon’s preference and using the same technique and equipment as those used to guide the FNA biopsy.
Results Our series included eight patients, four men and four women, 16–59 years old (mean [± SD] age, 45 ± 14 years). Seven patients had a history of head and neck cancer. Five patients had a history of papillary thyroid cancer (PTC), and the final diagnoses were three metastatic nodes, one benign reactive hyperplastic node, and one normal node. One patient had a history of medullary thyroid cancer, and the final diagnosis was metastatic medullary cancer. One patient had a history of esthesioneuroblastoma, and a previous CT-guided core biopsy had confirmed nodal metastatic disease (a CT-guided FNA biopsy was not diagnostic). In that case, transoral ultrasound was performed to intraoperatively localize the mass. One patient did not have a history of malignancy. In the course of his evaluation for
dysphagia at another facility, a retropharyngeal mass had been incidentally visualized on CT and MRI examinations. The transoral ultrasound–guided FNA biopsy diagnosed a ganglion cyst that was resected transorally. Lesions were detected on CT, MRI, or PET/CT examination. All eight patients underwent a CT examination; three underwent MRI, and one underwent PET/CT. Appearance of Lesions on Transoral Ultrasound Six lesions were located on the left side and two were on the right side of the retropharyngeal space. Their longest diameters ranged from 1.5 to 4.3 cm, with a mean of 2.4 ± 1.0 cm and a median of 2.1 cm. All lesions were hypoechoic. Cystic areas were noted in one ganglion cyst and in one of the three metastatic nodes identified in patients with PTC
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Fornage et al.
A
B
C
D
E
F
Fig. 4—58-year-old man with history of esthesioneuroblastoma of left nasal sinus. PET/CT showed uptake in region of right retropharyngeal space that was suspicious for metastatic retropharyngeal node, so patient underwent transoral ultrasound–guided intraoperative localization of metastatic node in retropharyngeal space. A, PET/CT scan reveals radiotracer uptake in right retropharyngeal space (arrow). B, CT scan shows suspicious enhancing node in right retropharyngeal space (arrow). Note length of path of needle (6.9 cm) during CT-guided needle biopsy (longer white line). CT-guided fine-needle aspiration (FNA) biopsy failed to yield diagnostic specimen, and CT-guided core biopsy was required to confirm metastatic nature of node. C, Sagittal oblique gray-scale transoral ultrasound scan shows elongated node (calipers). D, Transverse transoral ultrasound scan shows metastatic node (calipers) anterior to internal carotid artery (ICA). E, Transverse power Doppler transoral ultrasound scan shows flow in ICA (arrow) adjacent to metastatic node (arrowheads), as well as flow in small metastatic node. F, Photograph taken during intraoperative localization of node. Methylene blue was injected using same transoral ultrasound guidance as that used for FNA biopsy. Note additional marking of mucosa (arrow).
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Transoral Ultrasound of Retropharyngeal Masses
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(Fig. 3). Microcalcifications were seen in two of the three PTC nodal metastases. The ICA and IJV were unequivocally identified on color or power Doppler in all eight cases. FNA Biopsy Results Transoral ultrasound–guided FNA biopsy of the suspicious mass was performed in four of eight cases. In all four cases, including two cases of nodal metastases from PTC, one benign reactive hyperplasia, and one ganglion cyst, the specimen obtained with a single FNA pass was diagnostic. In the patient with a benign reactive hyperplastic node, a diagnosis of lymphoma was considered. For that reason, a transoral ultrasound– guided core biopsy was performed, which excluded lymphoma and confirmed the diagnosis of benign reactive lymphoid hyperplasia obtained on the FNA. This was also confirmed by flow cytometry that was used on the FNA sample to test for lymphoma markers; the results were negative for lymphoma. The patient moved to another state and was lost to follow-up. In the patient with the ganglion cyst, the cytologic diagnosis was confirmed by the pathologic examination of the lesion that was resected transorally during the same session, after the transoral ultrasound–guided FNA biopsy. There were no complications from the transoral ultrasound–guided FNAs and core biopsy. Six of the eight patients underwent minimally invasive transoral surgical excision. Of the two patients who did not undergo a resection, one had a suspicious node on PET/ CT and CT scans, but the transoral ultrasound–guided FNA and core biopsy results were negative for malignancy and consistent with benign reactive hyperplasia. In the other patient, transoral ultrasound revealed a small benign-appearing node that measured 0.6 cm on CT; this node has remained unchanged on CT scans for the past 3 years. Intraoperative Localization of Lesions Before Transoral Resection Three nonpalpable lesions were localized intraoperatively before their transoral resection using mucosal marking with a permanent marking pen. In one of these three cases (the patient with recurrent metastatic esthesioneuroblastoma), the mucosal marker was supplemented with an injection of methylene blue in the perilesional tissues at the surgeon’s request. In this patient, a CT-guided FNA biopsy of the suspicious node had failed to yield an adequate
specimen and a concomitant CT-guided core biopsy had been required to confirm the metastasis (Fig. 4). Discussion Recently, there has been renewed interest in a simple direct transoral surgical approach to excise retropharyngeal masses, especially lymph node metastases from thyroid cancer [5–7]. In patients with PTC, the complete resection of recurrent regional disease is correlated with improved disease-free survival; thus, an aggressive surgical approach is warranted to excise any isolated retropharyngeal lymph node metastases [8, 9]. When recurrent disease is limited to one retropharyngeal node, a minimally invasive transoral resection is preferred over the more difficult transcervical or transmandibular approach [5]. However, to ensure that minimally invasive surgery is possible, accurate preoperative imaging is required to show the relationship of the lesion with the adjacent vasculature and thus guide the surgeon. Transoral ultrasound, with its real-time and color Doppler capabilities, can provide this critical information. In all cases in our series, transoral ultrasound clearly revealed the relationship between the mass and the ICA and IJV. Transoral ultrasound with power Doppler imaging can also show the internal vascularity associated with the retropharyngeal mass. In all cases of Rouviere nodes, power Doppler revealed increased internal vascularity. In the case of the ganglion cyst, as expected, no flow was seen in the mass. Another prerequisite for performing transoral resection is preoperative confirmation of the nature of the mass. Transoral ultrasound–guided FNA biopsy (and core needle biopsy, if required and if space permits) can be used to preoperatively confirm metastasis in the node. On the basis of our experience, transoral ultrasound–guided FNA of retropharyngeal space masses is effective, and a single pass yielded adequate specimens in all cases. In one case, FNA biopsy was complemented by an 18-gauge core biopsy to rule out lymphoma. In that case, the node was large and the ICA and IJV were located at a safe distance, thus allowing the 2.3-cm throw of the cutting needle with no risk of injuring the vessels. Transoral ultrasound allows fast 2D ultrasound examination, with sonograms obtained in many directions. Switching from the sagittal to the transverse plane better reveals the relationship between the lesion and
the adjacent vessels. Real-time examination makes ultrasound uniquely superior to other cross-sectional imaging modalities. Operators should take advantage of this feature and use graded compression of the pharyngeal wall with the probe to assess the mobility and compressibility (firmness) of retropharyngeal masses. Using this dynamic examination technique, one can better assess the presence or absence of a fat plane between the lesion and the carotid artery, which is critical information for the surgeon before the excision. Cervical nodes involved with metastatic PTC present with cystic areas in 20% of cases [10]; in a patient with PTC, the presence of cystic areas should be highly suggestive (if not pathognomonic) of metastatic disease. In our series, one of three nodes involved with metastatic PTC contained cystic areas. The other case of cystic mass was a very rare case of ganglion cyst. Microcalcifications in a node are another hallmark of metastatic PTC. They are found in 50% of those metastatic nodes [10]. In our series, small calcifications were found in two of three metastatic PTC nodes. Intraoral ultrasound has been reported with the use of small-footprint finger-grip intraoperative probes that are placed in certain areas of the oral cavity. The main indications have been for the diagnosis of peritonsillar abscesses, the diagnosis of parapharyngeal masses, and the measurement of malignant tongue tumors [11–13]. Another recent specific application of intraoral ultrasound has been the diagnosis of calculi in salivary glands [14]. A high-frequency (25-MHz) handheld transducer has also been developed for dental examination of the teeth and gums [15]. In our first case, we began the ultrasound examination using a small-footprint finger-grip intraoperative transducer. However, it was immediately obvious that it could not be moved adequately when applied to the posterior pharyngeal wall (mainly because of the limited space in the oral cavity) and that it was not possible to switch easily from the sagittal to the transverse scan plane. In addition, such transducers would not provide easy transoral ultrasound guidance for needle biopsy. Therefore, we switched to rigid endocavitary transducers, whose end-firing viewing better suited the requirements for transoral ultrasound imaging and transoral ultrasound–guided FNA biopsy. Wong et al. [16] reported the successful use of intraoral ultrasound with a “hockeystick” transducer to visualize and biopsy
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Fornage et al. three relatively large deep-seated masses in the parapharyngeal region. They used a small hockey-stick linear-array transducer and a freehand FNA technique, which, in the case of small retropharyngeal space masses and because of the limited access to the target lesions, is more cumbersome than our biopsy technique. In contrast with the linear probe that was used by Wong et al., the use of an end-firing endocavitary probe with a wide-sector FOV allows imaging with a very small area of contact with the pharynx. More importantly, the use of the needle guide attached to the endocavitary probe does not require extra space and movements around the probe to align the needle with the probe’s scan plane. Instead, the use of the needle guide guarantees that the needle will follow the expected trajectory and its tip will appear within the target at first trial. A limitation of our study is the small number of cases. However, even with our small number of patients, the technique has proved to be simple and easy to perform. The major advantage of the technique is that the FNA biopsy is guided automatically and accurately by the attached needle guide. It therefore does not require the amount of expertise needed for ultrasound-guided needle biopsies with the hand-free technique, as in the study by Wong et al. [16]. In summary, the techniques of transoral ultrasound, transoral ultrasound–guided FNA biopsy, and intraoperative localization have proved useful to confirm the presence of a suspicious mass in the retropharyngeal space, obtain its pathologic diagnosis, and
facilitate its minimally invasive transoral resection. Transoral ultrasound–guided needle biopsy may replace the more complex and challenging CT-guided needle biopsy technique that has been required until now for this type of lesion. References 1. Kaplan SL, Mandel SJ, Muller R, Baloch ZW, Thaler ER, Loevner LA. The role of MR imaging in detecting nodal disease in thyroidectomy patients with rising thyroglobulin levels. AJNR 2009; 30:608–612 2. Otsuki N, Nishikawa T, Iwae S, Saito M, Mohri M, Nibu K. Retropharyngeal node metastasis from papillary thyroid carcinoma. Head Neck 2007; 29:508–511 3. Chu HR, Kim JH, Yoon DY, Hwang HS, Rho YS. Additional diagnostic value of 18F-FDG PET-CT in detecting retropharyngeal nodal metastases. Otolaryngol Head Neck Surg 2009; 141:633–638 4. Connor SE, Chaudhary N. CT-guided percutaneous core biopsy of deep face and skull-base lesions. Clin Radiol 2008; 63:986–994 5. Shellenberger T, Fornage B, Ginsberg L, Clayman GL. Transoral resection of thyroid cancer metastasis to lateral retropharyngeal nodes. Head Neck 2007; 29:258–266 6. Andrews GA, Kwon M, Clayman G, Edeiken B, Kupferman ME. Technical refinement of ultrasound-guided transoral resection of parapharyngeal/retropharyngeal thyroid carcinoma metastases. Head Neck 2011; 33:166–170 7. Le TD, Cohen JI. Transoral approach to removal of the retropharyngeal lymph nodes in welldifferentiated thyroid cancer. Laryngoscope 2007; 117:1155–1158 8. Ma QD, Grimm K, Paz BI, Maghami E. Transoral
surgical approach for retropharyngeal node involvement in I-131-negative 18-fluoro-2deoxyglucose positron emission tomographypositive recurrent thyroid cancer. Skull Base 2009; 19:431–436 9. Stojadinovic A, Shoup M, Nissan A, et al. Recurrent differentiated thyroid carcinoma: biological implications of age, method of detection, and site and extent of recurrence. Ann Surg Oncol 2002; 9:789–798 10. Rosário PW, de Faria S, Bicalho L, et al. Ultrasonographic differentiation between metastatic and benign lymph nodes in patients with papillary thyroid carcinoma. J Ultrasound Med 2005; 24:1385–1389 11. Lyon M, Blaivas M. Intraoral ultrasound in the diagnosis and treatment of suspected peritonsillar abscess in the emergency department. Acad Emerg Med 2005; 12:85–88 12. Rebol J, Takač I, Bumber Z. Intraoral sonographic evaluation of parapharyngeal space tumors. J Clin Ultrasound 2001; 29:302–305 13. Kodama M, Khanal A, Habu M, et al. Ultrasonography for intraoperative determination of tumor thickness and resection margin in tongue carcinomas. J Oral Maxillofac Surg 2010; 68:1746–1752 14. Cho W, Lim D, Park H. Transoral sonographic diagnosis of submandibular duct calculi. J Clin Ultrasound 2013; 42:125–128 15. Salmon B, Le Denmat D. Intraoral ultrasonography: development of a specific high-frequency probe and clinical pilot study. Clin Oral Investig 2012; 16:643–649 16. Wong KT, Tsang RK, Tse GM, Yuen EH, Ahuja AT. Biopsy of deep-seated head and neck lesions under intraoral ultrasound guidance. AJNR 2006; 27:1654–1657
F O R YO U R I N F O R M AT I O N
The data supplement accompanying this web exclusive article can be viewed by clicking “Supplemental” at the top of the article.
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Neuroradiology/Head and Neck Imaging Original Research
Use of Transoral Sonography With an Endocavitary Transducer in Diagnosis, Fine-Needle Aspiration Biopsy, and Intraoperative Localization of Retropharyngeal Masses Bruno D. Fornage1,2 Beth S. Edeiken1 Gary L. Clayman2 Fornage BD, Edeiken BS, Clayman GL
Keywords: fine-needle aspiration biopsy, retropharyngeal lymph node metastases, thyroid cancer, transoral, ultrasound DOI:10.2214/AJR.13.11398 Received June 17, 2013; accepted after revision September 23, 2013. 1 Department of Diagnostic Radiology, The University of Texas M. D. Anderson Cancer Center, Unit 1350, 1155 Pressler St, Houston, TX 77030-3721. Address correspondence to B. D. Fornage ([email protected]). 2 Department of Surgical Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX.
WEB This is a web exclusive article. Supplemental Data Available online at www.ajronline.org. AJR 2014; 202:W481–W486 0361–803X/14/2025–W481 © American Roentgen Ray Society
OBJECTIVE. The purpose of this article is to describe the use of transoral sonography in the diagnosis, fine-needle aspiration (FNA) biopsy, and intraoperative localization of retropharyngeal masses. MATERIALS AND METHODS. We reviewed images and data for eight patients with a retropharyngeal mass identified on CT, MRI, or PET/CT as being suspicious for a metastatic Rouviere node. Transoral ultrasound was performed using a commercially available endorectal or endovaginal transducer. Transoral ultrasound–guided FNA biopsy was performed using a needle guide attached to the transducer shaft. Color and power Doppler imaging were used to identify the internal carotid artery and jugular vein and to plan the safest path to the targeted mass. The mass was intraoperatively localized by marking the mucosa with a permanent marker or by injecting methylene blue. RESULTS. There were six patients with a history of thyroid cancer (five papillary cancers and one medullary cancer), one patient with a history of esthesioneuroblastoma, and one patient with no history of cancer. Transoral ultrasound imaging was successful in all eight patients. Transoral ultrasound–guided FNA biopsy was performed in four patients, and a satisfactory cytologic diagnosis was obtained in all cases, although in one of those four cases, an additional core biopsy with an 18-gauge needle was performed to completely rule out lymphoma. Six patients underwent a transoral resection of the lesion. In three of them, the lesion was localized intraoperatively by making a mark on the mucosa and in one case by adding transoral ultrasound–guided injection of methylene blue. CONCLUSION. Transoral ultrasound can be used to visualize, sample, and localize abnormal masses in the retropharyngeal space, such as metastatic Rouviere nodes in patients with a history of head and neck cancer.
T
he retropharyngeal space is a potential space limited by the buccopharyngeal fascia and pharyngeal constrictor muscles anteriorly and the alar layer of prevertebral fascia posteriorly. It communicates with the parapharyngeal space. A fibrous raphe divides it into two lateral compartments, each containing fibrofatty tissue and retropharyngeal nodes known as Rouviere nodes, which are located medially to the internal carotid artery. Rouviere nodes usually regress during early childhood, but they can be a site of metastatic disease in patients with certain head and neck cancers, especially thyroid cancer. When involved, these nodes are detected on CT, MRI, or PET/CT scans obtained during cancer follow-up or for other reasons [1–3].
Currently, when a mass is detected in the retropharyngeal space, a preoperative tissue diagnosis can be obtained only via a CT-guided biopsy with a difficult subzygomatic or retromaxillary approach [4]. Here, we describe the use of direct transoral ultrasound in the diagnosis, fine-needle aspiration (FNA) biopsy, and intraoperative localization of masses in the retropharyngeal space and report our preliminary findings in a series of eight patients. Materials and Methods This retrospective review included transoral ultrasound images and reports from eight patients in whom CT, MRI, or PET/CT had revealed a mass in the retropharyngeal space that had been initially identified as suspicious for a metastatic Rouviere node. The patients underwent transoral ultrasound–guided needle biopsy and/or minimally
AJR:202, May 2014 W481
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Fornage et al. invasive transoral resection. Three patients were included in two previous publications detailing the surgical technique of transoral resection [5, 6]. This review was approved by our institution’s institutional review board and was compliant with HIPAA regulations.
Transoral Ultrasound Examination of the Retropharyngeal Space The transoral ultrasound examination was performed in the operating room. All but one patient had been prepared for a possible transoral resection and were under general anesthesia; the remaining patient was examined under local anesthesia. The patient was intubated with an armored size 6 or 7 endotracheal tube that was retracted and stabilized with a standard McIvor type of oral retractor commonly used in tonsillar surgery. There was no interference between the endotracheal tube and the placement of the endocavitary probe (Fig. 1). We used an ultrasound scanner (Prosound α 10, Hitachi-Aloka) equipped with a 3.0- to-8.5-MHz endorectal probe (UST-675P, Hitachi-Aloka) in three patients and a 2.5- to-7.5-MHz endovaginal transducer (UST-9118, Hitachi-Aloka) in five patients. Both probes have an outer diameter of 2.3 cm at the tip (scan head) and offer an end-firing 180° FOV. In the first patient, an attempt had also been made to use an intraoperative 3.75- to-10.0-MHz curved-array small-footprint finger-grip probe (UST 9132I, Hitachi-Aloka) with a 70° scanning angle. After its last use, the transducer was sterilized by being immersed in a 0.55% solution of ortho-phthalaldehyde (Cidex OPA, Ethicon) for 15 minutes, followed by gas sterilization with hydrogen peroxide gas for 1 hour. The endocavitary probe was fitted with a dedicated probe cover (NeoGuard, Civco Medical Solutions) after a small amount of sterile coupling gel had been deposited on the scan head. No coupling gel was necessary on the outside of the covered probe because the normal secretions covering the pharyngeal mucosa were sufficient to obtain a satisfactory acoustic coupling and images of good quality. Gray-scale and color and power Doppler imaging were used in all examinations. On occasion, transducer compression was applied through the pharyngeal wall so that the deformability of the lesion could be appreciated. Orthogonal (usually longitudinal but sometimes sagittal oblique and transverse) sonograms were obtained of each lesion. All lesions were measured, and their echogenicity and echotexture were evaluated, especially for the presence of cystic areas and microcalcifications. Color and power Doppler imaging were used to identify the internal carotid artery (ICA) and internal jugular vein (IJV) and to evaluate lesions’ internal vascularity after optimizing the color Doppler settings (mostly the pulse repetition frequency) of the scanner.
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Fig. 1—Intraoperative setting. Photograph shows that oral retractor is in place, and soft palate has been retracted with soft rubber catheter. Endocavitary probe has been inserted in oral cavity.
Ultrasound-Guided FNA Biopsy of Retropharyngeal Space Masses A metallic needle guide (MP-2748 for the UST9118 endovaginal probe or MP-2452 for the UST675P endorectal probe, all from Hitachi-Aloka) was attached securely along the shaft of the endocavitary probe (Fig. 2). The guide has been designed so that the needle is completely included in the sector scan plane after it exits the guide. A 25cm 20-gauge needle was used to accommodate the length of the needle guide. The probe equipped with the needle guide was inserted in the oral cavity, and its extremity was placed in direct contact with the pharyngeal mucosa. A gray-scale sonogram of the retropharyngeal space appeared on the monitor. Color or power Doppler ultrasound was used to identify the ICA and IJV. A built-in electronic biopsy line was activated and superimposed on the gray-scale sonogram to indicate the expected trajectory of the needle. The position of the transducer was adjusted so that the biopsy line would cross the suspicious mass. The needle was then inserted through the guide. Mild resistance was felt as the needle tip came into contact with the pharyngeal wall. Although the 20-gauge needle has a sharp bevel, a short thrust was often needed to pierce the wall. The needle then entered the sector FOV and appeared as a brightly echogenic line (see Video S1, which can be viewed by clicking Supplemental at the top of this article and then clicking the video number on the Supplemental page). The clear visualization of the needle tip allowed the operator to keep it within the limits of the target lesion during the FNA biopsy and at a safe distance from the ICA and IJV. Cellular material was aspirated from the retropharyngeal space mass by applying moderate (1–2 mL) but continuous negative pressure using the hand holding the syringe while holding the transducer in place with the other hand. The aspiration process lasted about 20–30 seconds, during which the needle was moved to and fro to mechanically
tear off and aspirate sheaths of cells from the lesion and to increase the volume of the aspirate. Because of the length of the needle, the appearance of blood-tinged material in the hub guaranteed that the aspirated material was quantitatively adequate because the whole length of the needle would be filled with cellular material. Aspiration was then stopped, and after the suction had been released, the needle-syringe assembly was pulled out of the needle guide. The cellular aspirate was recovered from the needle and smeared on a few slides. All smears were prepared by the radiologist; the slides were fixed and sent to the cytopathology laboratory, where they were stained using a Romanowsky stain (DiffQuick, Fisher Scientific) technique. A cytopathologist was available to provide a preliminary diagnosis within 15 minutes. In one case, the transoral ultra-
Fig. 2—Photograph shows endocavitary probe equipped with needle guide for needle biopsy. Dotted line indicates trajectory of needle.
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Transoral Ultrasound of Retropharyngeal Masses
A
B Fig. 3—59-year-old woman with history of papillary thyroid cancer and metastatic Rouviere node. A, Transverse gray-scale sonogram of left retropharyngeal space shows enlarged node with internal cystic areas (arrows) adjacent to internal carotid artery (ICA). B, Longitudinal sonogram shows node in its longest axis and shows cluster of microcalcifications (arrow) in addition to cystic areas. C, Power Doppler sonogram shows ICA adjacent to node. Note increased vascularity in metastatic node.
C sound–guided FNA biopsy was followed by a core needle biopsy, performed using the same type of transoral ultrasound guidance and an 18-gauge disposable automated biopsy device (Maxcore, Bard). The final diagnosis of malignancy was based on the cytopathological diagnosis. Clinical or imaging follow-up data were obtained for the patients with a benign cytopathological diagnosis.
Intraoperative Localization of Lesions Before Transoral Resection In selected cases, the retropharyngeal space mass was localized intraoperatively with transoral ultrasound before transoral resection using a simple marking of the lesion projection on the pharyngeal mucosa with a permanent marker or the injection of a small amount (< 1 mL) of methylene blue into the perilesional tissues according to the surgeon’s preference and using the same technique and equipment as those used to guide the FNA biopsy.
Results Our series included eight patients, four men and four women, 16–59 years old (mean [± SD] age, 45 ± 14 years). Seven patients had a history of head and neck cancer. Five patients had a history of papillary thyroid cancer (PTC), and the final diagnoses were three metastatic nodes, one benign reactive hyperplastic node, and one normal node. One patient had a history of medullary thyroid cancer, and the final diagnosis was metastatic medullary cancer. One patient had a history of esthesioneuroblastoma, and a previous CT-guided core biopsy had confirmed nodal metastatic disease (a CT-guided FNA biopsy was not diagnostic). In that case, transoral ultrasound was performed to intraoperatively localize the mass. One patient did not have a history of malignancy. In the course of his evaluation for
dysphagia at another facility, a retropharyngeal mass had been incidentally visualized on CT and MRI examinations. The transoral ultrasound–guided FNA biopsy diagnosed a ganglion cyst that was resected transorally. Lesions were detected on CT, MRI, or PET/CT examination. All eight patients underwent a CT examination; three underwent MRI, and one underwent PET/CT. Appearance of Lesions on Transoral Ultrasound Six lesions were located on the left side and two were on the right side of the retropharyngeal space. Their longest diameters ranged from 1.5 to 4.3 cm, with a mean of 2.4 ± 1.0 cm and a median of 2.1 cm. All lesions were hypoechoic. Cystic areas were noted in one ganglion cyst and in one of the three metastatic nodes identified in patients with PTC
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Fornage et al.
A
B
C
D
E
F
Fig. 4—58-year-old man with history of esthesioneuroblastoma of left nasal sinus. PET/CT showed uptake in region of right retropharyngeal space that was suspicious for metastatic retropharyngeal node, so patient underwent transoral ultrasound–guided intraoperative localization of metastatic node in retropharyngeal space. A, PET/CT scan reveals radiotracer uptake in right retropharyngeal space (arrow). B, CT scan shows suspicious enhancing node in right retropharyngeal space (arrow). Note length of path of needle (6.9 cm) during CT-guided needle biopsy (longer white line). CT-guided fine-needle aspiration (FNA) biopsy failed to yield diagnostic specimen, and CT-guided core biopsy was required to confirm metastatic nature of node. C, Sagittal oblique gray-scale transoral ultrasound scan shows elongated node (calipers). D, Transverse transoral ultrasound scan shows metastatic node (calipers) anterior to internal carotid artery (ICA). E, Transverse power Doppler transoral ultrasound scan shows flow in ICA (arrow) adjacent to metastatic node (arrowheads), as well as flow in small metastatic node. F, Photograph taken during intraoperative localization of node. Methylene blue was injected using same transoral ultrasound guidance as that used for FNA biopsy. Note additional marking of mucosa (arrow).
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Transoral Ultrasound of Retropharyngeal Masses
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(Fig. 3). Microcalcifications were seen in two of the three PTC nodal metastases. The ICA and IJV were unequivocally identified on color or power Doppler in all eight cases. FNA Biopsy Results Transoral ultrasound–guided FNA biopsy of the suspicious mass was performed in four of eight cases. In all four cases, including two cases of nodal metastases from PTC, one benign reactive hyperplasia, and one ganglion cyst, the specimen obtained with a single FNA pass was diagnostic. In the patient with a benign reactive hyperplastic node, a diagnosis of lymphoma was considered. For that reason, a transoral ultrasound– guided core biopsy was performed, which excluded lymphoma and confirmed the diagnosis of benign reactive lymphoid hyperplasia obtained on the FNA. This was also confirmed by flow cytometry that was used on the FNA sample to test for lymphoma markers; the results were negative for lymphoma. The patient moved to another state and was lost to follow-up. In the patient with the ganglion cyst, the cytologic diagnosis was confirmed by the pathologic examination of the lesion that was resected transorally during the same session, after the transoral ultrasound–guided FNA biopsy. There were no complications from the transoral ultrasound–guided FNAs and core biopsy. Six of the eight patients underwent minimally invasive transoral surgical excision. Of the two patients who did not undergo a resection, one had a suspicious node on PET/ CT and CT scans, but the transoral ultrasound–guided FNA and core biopsy results were negative for malignancy and consistent with benign reactive hyperplasia. In the other patient, transoral ultrasound revealed a small benign-appearing node that measured 0.6 cm on CT; this node has remained unchanged on CT scans for the past 3 years. Intraoperative Localization of Lesions Before Transoral Resection Three nonpalpable lesions were localized intraoperatively before their transoral resection using mucosal marking with a permanent marking pen. In one of these three cases (the patient with recurrent metastatic esthesioneuroblastoma), the mucosal marker was supplemented with an injection of methylene blue in the perilesional tissues at the surgeon’s request. In this patient, a CT-guided FNA biopsy of the suspicious node had failed to yield an adequate
specimen and a concomitant CT-guided core biopsy had been required to confirm the metastasis (Fig. 4). Discussion Recently, there has been renewed interest in a simple direct transoral surgical approach to excise retropharyngeal masses, especially lymph node metastases from thyroid cancer [5–7]. In patients with PTC, the complete resection of recurrent regional disease is correlated with improved disease-free survival; thus, an aggressive surgical approach is warranted to excise any isolated retropharyngeal lymph node metastases [8, 9]. When recurrent disease is limited to one retropharyngeal node, a minimally invasive transoral resection is preferred over the more difficult transcervical or transmandibular approach [5]. However, to ensure that minimally invasive surgery is possible, accurate preoperative imaging is required to show the relationship of the lesion with the adjacent vasculature and thus guide the surgeon. Transoral ultrasound, with its real-time and color Doppler capabilities, can provide this critical information. In all cases in our series, transoral ultrasound clearly revealed the relationship between the mass and the ICA and IJV. Transoral ultrasound with power Doppler imaging can also show the internal vascularity associated with the retropharyngeal mass. In all cases of Rouviere nodes, power Doppler revealed increased internal vascularity. In the case of the ganglion cyst, as expected, no flow was seen in the mass. Another prerequisite for performing transoral resection is preoperative confirmation of the nature of the mass. Transoral ultrasound–guided FNA biopsy (and core needle biopsy, if required and if space permits) can be used to preoperatively confirm metastasis in the node. On the basis of our experience, transoral ultrasound–guided FNA of retropharyngeal space masses is effective, and a single pass yielded adequate specimens in all cases. In one case, FNA biopsy was complemented by an 18-gauge core biopsy to rule out lymphoma. In that case, the node was large and the ICA and IJV were located at a safe distance, thus allowing the 2.3-cm throw of the cutting needle with no risk of injuring the vessels. Transoral ultrasound allows fast 2D ultrasound examination, with sonograms obtained in many directions. Switching from the sagittal to the transverse plane better reveals the relationship between the lesion and
the adjacent vessels. Real-time examination makes ultrasound uniquely superior to other cross-sectional imaging modalities. Operators should take advantage of this feature and use graded compression of the pharyngeal wall with the probe to assess the mobility and compressibility (firmness) of retropharyngeal masses. Using this dynamic examination technique, one can better assess the presence or absence of a fat plane between the lesion and the carotid artery, which is critical information for the surgeon before the excision. Cervical nodes involved with metastatic PTC present with cystic areas in 20% of cases [10]; in a patient with PTC, the presence of cystic areas should be highly suggestive (if not pathognomonic) of metastatic disease. In our series, one of three nodes involved with metastatic PTC contained cystic areas. The other case of cystic mass was a very rare case of ganglion cyst. Microcalcifications in a node are another hallmark of metastatic PTC. They are found in 50% of those metastatic nodes [10]. In our series, small calcifications were found in two of three metastatic PTC nodes. Intraoral ultrasound has been reported with the use of small-footprint finger-grip intraoperative probes that are placed in certain areas of the oral cavity. The main indications have been for the diagnosis of peritonsillar abscesses, the diagnosis of parapharyngeal masses, and the measurement of malignant tongue tumors [11–13]. Another recent specific application of intraoral ultrasound has been the diagnosis of calculi in salivary glands [14]. A high-frequency (25-MHz) handheld transducer has also been developed for dental examination of the teeth and gums [15]. In our first case, we began the ultrasound examination using a small-footprint finger-grip intraoperative transducer. However, it was immediately obvious that it could not be moved adequately when applied to the posterior pharyngeal wall (mainly because of the limited space in the oral cavity) and that it was not possible to switch easily from the sagittal to the transverse scan plane. In addition, such transducers would not provide easy transoral ultrasound guidance for needle biopsy. Therefore, we switched to rigid endocavitary transducers, whose end-firing viewing better suited the requirements for transoral ultrasound imaging and transoral ultrasound–guided FNA biopsy. Wong et al. [16] reported the successful use of intraoral ultrasound with a “hockeystick” transducer to visualize and biopsy
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Fornage et al. three relatively large deep-seated masses in the parapharyngeal region. They used a small hockey-stick linear-array transducer and a freehand FNA technique, which, in the case of small retropharyngeal space masses and because of the limited access to the target lesions, is more cumbersome than our biopsy technique. In contrast with the linear probe that was used by Wong et al., the use of an end-firing endocavitary probe with a wide-sector FOV allows imaging with a very small area of contact with the pharynx. More importantly, the use of the needle guide attached to the endocavitary probe does not require extra space and movements around the probe to align the needle with the probe’s scan plane. Instead, the use of the needle guide guarantees that the needle will follow the expected trajectory and its tip will appear within the target at first trial. A limitation of our study is the small number of cases. However, even with our small number of patients, the technique has proved to be simple and easy to perform. The major advantage of the technique is that the FNA biopsy is guided automatically and accurately by the attached needle guide. It therefore does not require the amount of expertise needed for ultrasound-guided needle biopsies with the hand-free technique, as in the study by Wong et al. [16]. In summary, the techniques of transoral ultrasound, transoral ultrasound–guided FNA biopsy, and intraoperative localization have proved useful to confirm the presence of a suspicious mass in the retropharyngeal space, obtain its pathologic diagnosis, and
facilitate its minimally invasive transoral resection. Transoral ultrasound–guided needle biopsy may replace the more complex and challenging CT-guided needle biopsy technique that has been required until now for this type of lesion. References 1. Kaplan SL, Mandel SJ, Muller R, Baloch ZW, Thaler ER, Loevner LA. The role of MR imaging in detecting nodal disease in thyroidectomy patients with rising thyroglobulin levels. AJNR 2009; 30:608–612 2. Otsuki N, Nishikawa T, Iwae S, Saito M, Mohri M, Nibu K. Retropharyngeal node metastasis from papillary thyroid carcinoma. Head Neck 2007; 29:508–511 3. Chu HR, Kim JH, Yoon DY, Hwang HS, Rho YS. Additional diagnostic value of 18F-FDG PET-CT in detecting retropharyngeal nodal metastases. Otolaryngol Head Neck Surg 2009; 141:633–638 4. Connor SE, Chaudhary N. CT-guided percutaneous core biopsy of deep face and skull-base lesions. Clin Radiol 2008; 63:986–994 5. Shellenberger T, Fornage B, Ginsberg L, Clayman GL. Transoral resection of thyroid cancer metastasis to lateral retropharyngeal nodes. Head Neck 2007; 29:258–266 6. Andrews GA, Kwon M, Clayman G, Edeiken B, Kupferman ME. Technical refinement of ultrasound-guided transoral resection of parapharyngeal/retropharyngeal thyroid carcinoma metastases. Head Neck 2011; 33:166–170 7. Le TD, Cohen JI. Transoral approach to removal of the retropharyngeal lymph nodes in welldifferentiated thyroid cancer. Laryngoscope 2007; 117:1155–1158 8. Ma QD, Grimm K, Paz BI, Maghami E. Transoral
surgical approach for retropharyngeal node involvement in I-131-negative 18-fluoro-2deoxyglucose positron emission tomographypositive recurrent thyroid cancer. Skull Base 2009; 19:431–436 9. Stojadinovic A, Shoup M, Nissan A, et al. Recurrent differentiated thyroid carcinoma: biological implications of age, method of detection, and site and extent of recurrence. Ann Surg Oncol 2002; 9:789–798 10. Rosário PW, de Faria S, Bicalho L, et al. Ultrasonographic differentiation between metastatic and benign lymph nodes in patients with papillary thyroid carcinoma. J Ultrasound Med 2005; 24:1385–1389 11. Lyon M, Blaivas M. Intraoral ultrasound in the diagnosis and treatment of suspected peritonsillar abscess in the emergency department. Acad Emerg Med 2005; 12:85–88 12. Rebol J, Takač I, Bumber Z. Intraoral sonographic evaluation of parapharyngeal space tumors. J Clin Ultrasound 2001; 29:302–305 13. Kodama M, Khanal A, Habu M, et al. Ultrasonography for intraoperative determination of tumor thickness and resection margin in tongue carcinomas. J Oral Maxillofac Surg 2010; 68:1746–1752 14. Cho W, Lim D, Park H. Transoral sonographic diagnosis of submandibular duct calculi. J Clin Ultrasound 2013; 42:125–128 15. Salmon B, Le Denmat D. Intraoral ultrasonography: development of a specific high-frequency probe and clinical pilot study. Clin Oral Investig 2012; 16:643–649 16. Wong KT, Tsang RK, Tse GM, Yuen EH, Ahuja AT. Biopsy of deep-seated head and neck lesions under intraoral ultrasound guidance. AJNR 2006; 27:1654–1657
F O R YO U R I N F O R M AT I O N
The data supplement accompanying this web exclusive article can be viewed by clicking “Supplemental” at the top of the article.
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