Ultrasound-Guided Transcutaneous Needle Biopsy of the Base of the Tongue and Floor of the Mouth From a Submental Approach

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1 TECHNICAL INNOVATION Ultrasound-Guided Transcutaneous Needle Biopsy of the Base of the Tongue and Floor of the Mouth From a Submental Approach Jason M. Wagner, MD, Rachel D. Conrad, MD, Trinitia Y. Cannon, MD, Anthony M. Alleman, MD Limited data exist regarding the feasibility of ultrasound-guided transcutaneous biopsy of the base of the tongue and floor of the mouth. This retrospective study reviewed 8 cases with lesions in the base of the tongue or floor of the mouth that were biopsied by fine-needle aspiration. Core biopsy was also needed in 1 case. All biopsies were technically successful, and all yielded squamous cell. One biopsy yielded a falsepositive result, as subsequent resection yielded high-grade dysplasia with no invasion. The other biopsy results were considered true-positive based on subsequent pathologic examinations (2 cases) or clinical/imaging follow-up (5 cases). There were no significant complications associated with the biopsies. Key Words base of the tongue; floor of the mouth; head and neck ultrasound; squamous cell cancer; ultrasound-guided biopsy Received June 3, 2015, from the Departments of Radiological Sciences (J.M.W., A.M.A.), Pathology (R.D.C.), and Otorhinolaryngology (T.Y.C.), Oklahoma University Health Sciences Center, Oklahoma City, Oklahoma USA. Revision requested June 22, Revised manuscript accepted for publication August 17, Address correspondence to Jason M. Wagner, MD, Department of Radiological Sciences, Oklahoma University Health Sciences Center, 940 NE 13th St, 4G-4250, Oklahoma City, OK USA. jason-wagner@ouhsc.edu Abbreviations CT, computed tomography; PET, positron emission tomography doi: /ultra S quamous cell of the floor of the mouth and base of the tongue is a common condition that contributes substantially to the worldwide burden of morbidity and mortality. 1,2 Patients with suspected primary or recurrent cancer in these locations require rapid tissue diagnosis to guide management. In most cases, potential tumors in these locations are successfully biopsied with standard surgical techniques. Alternatively, in patients who present with nodal metastatic disease in the neck, needle biopsy of the metastatic lesion is commonly performed. Occasionally, a patient will present with a suspicious lesion in the base of the tongue or floor of the mouth without nodal metastatic disease, for which a standard surgical biopsy is either not successful or not feasible. When faced with this situation, we have performed ultrasound-guided transcutaneous needle biopsy using a submental approach. There are limited data available regarding the feasibility and safety of this biopsy approach. 3,4 The purpose of this study was to review our experience with transcutaneous biopsy of lesions in the base of the tongue and floor of the mouth using a submental approach by the American Institute of Ultrasound in Medicine J Ultrasound Med 2016; 35:

2 Materials and Methods This Health Insurance Portability and Accountability Act compliant retrospective study was approved by the Oklahoma University Health Sciences Center Institutional Review Board, and the requirement for informed consent was waived. All ultrasound-guided head and neck biopsy procedures performed by the Department of Radiology at the University of Oklahoma between January 1, 2011, and December 31, 2014, were reviewed by a single radiologist (J.M.W.), and 8 procedures targeting lesions in the base of the tongue or floor of the mouth were identified. All relevant clinical, imaging, and pathologic records for these 8 patients were then reviewed by a radiologist specializing in head and neck imaging (A.M.A.), a pathologist specializing in cytopathology (R.D.C.), and an otolaryngologist specializing in head and neck oncologic surgery (T.Y.C.). All biopsy procedures were performed by a single operator (J.M.W.) with real-time ultrasound guidance using an iu22 ultrasound system (Philips Healthcare, Andover MA). Linear (L12-5) or small curved (C8-5) transducers were used as appropriate for the patient. The patients were positioned either supine or sitting up to 70 upright, as was comfortable for the patient. The neck was extended to the extent tolerated, and the targeted lesion was visualized. The transducers were held in a transverse orientation posterior to the mentum of the mandible and angled posterior-superior to produce an oblique coronal plane. Ultrasound-guided fine-needle aspiration was performed with 25- or 22-gauge needles of the appropriate length for each case. On average, 3 needle passes were performed (range, 1 5). The needle trajectory was optimized for each patient but generally was medial to lateral. The initial needle pass was performed without suction. Manual suction was added on subsequent needle passes if the initial sample was inadequate. With each needle pass, material was reviewed by a cytopathologist to determine adequacy. In 1 case, the material was not adequate, and 2 core biopsy samples were obtained under ultrasound guidance with an 18-gauge Biopince end-core type automated needle set to a 13-mm throw (Argon Medical Devices, Plano, TX). All patients received 1% lidocaine with epinephrine, injected under ultrasound guidance, for local anesthesia. Three patients also received moderate conscious sedation. Results Of the 1512 ultrasound-guided head and neck needle biopsies performed by the Department of Radiology at our institution during the 4-year study period, only 8 procedures (0.5%) targeted lesions in the base of the tongue or floor of the mouth. The 8 patients consisted of 2 women and 6 men with an average age of 61 years (range, years). The characteristics of the patients and procedures are given in Table 1. All patients had a suspicious lesion in the base of the tongue or floor of the mouth, which was shown on computed tomography (CT) or positron emission tomography (PET)/CT (Figure 1). Three patients had negative surgical biopsy results with a persistent clinical concern for cancer. Three patients could not successfully undergo surgical biopsy because the lesions were not clinically visible. Two patients were poor candidates for surgical biopsy. Two patients also had suspicious cervical lymph nodes. In both cases (patients 2 and 8), the nodes were biopsied first. The preliminary cytopathologic results (and subsequent final pathologic results) in both cases were negative for malignancy; therefore, biopsy of the base of the tongue was performed. The remaining 6 patients either had no nodal disease or had nodal disease, but the presence or absence of recurrent malignancy in the base of the tongue had to be established to determine appropriate management. All 8 procedures were technically successful, and all yielded pathologic material that was interpreted as consistent with squamous cell. In 1 case (patient 8), the result was false-positive, as the subsequent partial glossectomy specimen was found to have high-grade dysplasia without invasion. This patient was the only one in our series who did not have a prior pathologic diagnosis of squamous cell. This patient presented with a painful tongue lesion that was highly suspicious on CT, and the result of a prior surgical biopsy performed at another institution, which yielded only benign tissue, was thought to potentially be a false-negative finding. One patient (patient 1) had a hemiglossectomy after the biopsy, which confirmed recurrent squamous cell. One patient with recurrent cancer in the base of the tongue had progression of disease, with a biopsy confirming nodal metastasis 9 months after the base-of-the-tongue biopsy. The other 5 patients had no further biopsies; however, review of all available clinical and imaging records showed disease courses consistent with recurrent cancer. Thus, 7 of the 8 cases (87.5%) were considered to have true-positive results. There were no major complications arising from the biopsy procedures. One patient reported pain after the biopsy, which subsequently resolved J Ultrasound Med 2016; 35:

3 Discussion The ability of transcutaneous ultrasound imaging to visualize malignant tumors of the tongue has been recognized for more than 35 years. 5 7 In this study, we found the targeted lesions to be solid in appearance and hypoechoic relative to surrounding tissues, particularly the intrinsic muscles of the tongue, which tended to be hyperechoic. Adjacent structures visible with ultrasound, including the hyoid bone and lingual arteries, were useful landmarks for localizing the lesions. Although ultrasound-guided biopsy of head and neck lymph nodes, thyroid nodules, and major salivary gland lesions is well established, there are very little published data regarding the feasibility or safety of ultrasound-guided biopsy of lesions in the base of the tongue and floor of the mouth. Meacham et al 3 performed a cadaveric feasibility study and found needle placement in the base of the tongue with injection of dye to be successful in 25 of 32 attempts (78%). The authors of that study appear to have used a through-plane guidance technique, in which the needle is placed along the center of the long edge of the transducer, and only a small portion of the shaft of the needle is visible. We use an in-plane guidance technique, in which the needle is placed along the short edge of transducer, and most of the needle shaft is visible. Chen et al 4 recently reported a series of 10 patients with tumors in the base of the tongue that were successfully biopsied by transcutaneous ultrasound-guided core biopsy. In our series, all patients initially had fine-needle aspiration, which was considered diagnostic on preliminary cytopathologic review in 7 of 8 cases. Only 1 of 8 cases required core biopsy because of an inadequate fine-needle aspirate. Although both our study and the study by Chen et al 4 found no major complications, the fine-needle aspiration technique uses a smaller needle without a cutting mechanism and, therefore, has a theoretically lower risk of complications. A disadvantage of fine-needle aspiration is that less tissue is collected than with core biopsy, and a pathologist with expertise in cytopathology is required for accurate interpretation. Another potential limitation of fine-needle aspiration is the fact that thin needles can be more difficult to visualize with ultrasound at the depth required for biopsy of the base of the tongue compared to larger core biopsy needles. Although ultrasound guidance for needle biopsy of superficial structures in the head and neck is well established, CT guidance is generally advocated for biopsy of Table 1 Characteristics of 8 Patients Who Underwent Ultrasound-Guided Transcutaneous Biopsy of Lesions in the Base of the Tongue and Floor of the Mouth Patient/Age, Lesion Lesion Prior Subsequent y/sex History Location Size, cm Imaging Indication Biopsy Result Pathologic Result 1/74/male Floor of mouth Deep floor 3.2 Neck CT No visible lesion Squamous cell Squamous cell squamous cell of mouth confirmed at excision 2/56/male Base of tongue Base of tongue 1.0 PET/CT Negative surgical Squamous cell None squamous cell biopsy 3/48/female Oral tongue Base of tongue 3.0 PET/CT Negative surgical Squamous cell None squamous cell biopsy 4/70/male Laryngeal Deep floor 2.4 PET/CT Excessive Squamous cell None squamous cell of mouth surgical risk 5/56/male Base of tongue Base of tongue 1.8 PET/CT No visible Squamous cell Metastatic squamous squamous cell lesion cell in level 1b lymph node 9 mo later 6/60/male Laryngeal Base of tongue 1.8 PET/CT Surgical biopsy Squamous cell None squamous cell not feasible 7/59/female Base of tongue Lateral base 1.5 PET/CT No visible lesion Squamous cell None squamous cell of tongue 8/64/male No prior cancer Base of tongue 1.6 Neck CT Negative surgical Squamous cell High-grade dysplasia diagnosis biopsy at partial glossectomy J Ultrasound Med 2016; 35:

4 Figure 1. Recurrent squamous cell in the base of the tongue in a 56-year-old man (patient 2). A, Fused axial PET/CT showing a focus of hypermetabolism (arrow) that was suspicious for recurrent. B, Transverse submental ultrasound image showing a 22-gauge needle (short arrows) within the hypoechoic lesion (long arrow). deep structures, including lesions at the skull base and in the parapharyngeal space. 8 Ultrasound has multiple advantages over CT guidance in the base-of-the-tongue region, including nonaxial plane guidance, the ability to visualize tongue tumors without contrast, and the lack of artifacts from dental amalgams. Doppler techniques allow the visualization and avoidance of relevant vascular structures (Figure 2). Finally, ultrasound has the benefit of real-time imaging to compensate for motion of the jaw and tongue. In fact, we use tissue motion induced by high-frequency, low-amplitude shaking of the needle to help guide the needle through deep, echogenic tongue tissue. This study had several limitations, including its retrospective design, the small number of patients, and the lack of subsequent pathologic confirmation in 5 of 8 cases. The small number of patients was expected, as transcutaneous biopsy of the base of the tongue and floor of the mouth is only currently indicated in patients who cannot be successfully biopsied by standard surgical techniques and have no nodal or distant disease that is amenable to biopsy. Our approach of fine-needle aspiration with core biopsy only if needed requires the immediate availability of a cytopathologist and may not be feasible in many practice settings. Finally, ultrasound guidance techniques have a learning curve, and biopsy of the base of the tongue can be technically demanding. Figure 2. Squamous cell in the base of the tongue in a 60- year-old man (patient 6). A, Transverse submental color and pulsed Doppler image showing the right lingual artery at the lateral aspect of a mass (arrows) in the right base of the tongue. B, Transverse submental ultrasound image showing a 22-gauge needle (short arrows) within the mass (long arrows) 1012 J Ultrasound Med 2016; 35:

5 In conclusion, we found ultrasound-guided transcutaneous biopsy of masses in the base of the tongue and floor of the mouth to be technically feasible and safe. We consider this technique to be a good option when standard surgical biopsy techniques are either not successful or not feasible. References 1. Aiken AH. Pitfalls in the staging of oral cavity cancer. Neuroimaging Clin North Am 2013; 23: Corey A. Pitfalls in the staging of oropharyngeal squamous cell. Neuroimaging Clin North Am 2013; 23: Meacham RK, Boughter JD Jr, Sebelik ME. Ultrasound-guided fine-needle aspiration of the tongue base: a cadaver feasibility study. Otolaryngol Head Neck Surg 2012; 147: Chen CN, Lin CY, Ko JY, et al. Application of ultrasound-guided core biopsy as a novel diagnostic tool for base of tongue cancer: our experiences with ten patients. Clin Otolaryngol 2016; 41: Mettler FA, Schultz K, Kelsey CA, Khan K, Sala J, Kligerman M. Grayscale ultrasonography in the evaluation of neoplastic invasion of the base of the tongue. Radiology 1979; 133: Fruehwald F, Salomonowitz E, Neuhold A, Pavelka R, Mailath G. Tongue Cancer: sonographic assessment of tumor stage. J Ultrasound Med 1987; 6: Blanco RG, Califano J, Messing B, et al. Transcervical ultrasonography is feasible to visualize and evaluate base of tongue cancers. PloS One 2014; 9:e Loevner LA. Image-guided procedures of the head and neck: the radiologist s arsenal. Otolaryngol Clin North Am 2008; 41: , viii. J Ultrasound Med 2016; 35: