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Surgical management of the base of tongue

      Lesions of the base of tongue (BOT) present a considerable challenge to the head and neck surgeon. This area represents a 3-dimensional anatomic region that is integral to both speech and swallow functions in addition to forming an important part of the upper respiratory tract. Surgical access to this region is difficult, and is primarily dictated by the size and type of lesion involving the BOT. The head and neck surgeon must be adept in the full spectrum of surgical techniques available to access the BOT, while keeping in mind the associated impact of each procedure on both form and function. Such techniques include transoral procedures, suprahyoid pharyngotomy, lip-split mandibulotomy or mandibular swing, and pull-through procedures. This article describes these techniques and considers the advantages and disadvantages of each.

      Keywords

      The base of tongue (BOT) is a 3-dimensional anatomic region within the upper aerodigestive tract that is intricately involved in respiration, articulation, and deglutition. The circumvallate papillae form the anterior anatomic and embryologic boundary, thus separating the pharyngeal BOT from the oral tongue.
      • Moore E.J.
      • Janus J.
      • Kasperbauer J.
      Transoral robotic surgery of the oropharynx: clinical and anatomical considerations.
      The BOT is further defined laterally by the glossopalatine sulci and posteriorly or inferiorly by the vallecula and pharyngoepiglottic folds. This muscular organ is composed of both intrinsic and extrinsic musculature that is lined by a complex mucosa containing squamous epithelium, minor salivary glands, and lymphoid tissue. The complexity of this mucosa in addition to the deep musculature and associated neurovascular structures leads to a diverse array pathologies associated with the BOT. One of the most common tumors arising in this location is malignant squamous cell carcinoma; however, the differential diagnosis is broad and includes normal lymphatic tissue, lymphoma, infections such as tuberculosis, granular cell tumors, salivary gland tumors (both benign and malignant), rhabdomyosarcoma, as well as metastatic disease.
      • Kim S.H.
      • Han M.H.
      • Park S.W.
      • et al.
      Radiologic-pathologic correlation of unusual lingual masses: part II: Benign and malignant tumors.
      In addition, benign processes such as ectopic lingual thyroid,

      Van Abel KM, Carlson ML, Boettcher NL, et al: Management algorithm for ectopic lingual thyroid including TORS thyroidectomy. Presented as a poster at the Combined Otolaryngology Society Meeting in Chicago, IL, April 2011.

      ectopic gastric mucosa,
      • Van Abel K.M.
      • Carlson M.L.
      • Narendra S.
      • et al.
      Hypopharyngeal gastric choristoma in an infant resulting in airway obstruction.
      and schwannomas must be considered.
      • Sawhney R.
      • Carron M.A.
      • Mathog R.H.
      Tongue base schwannoma: report, review, and unique surgical approach.
      Surgery as a primary modality is an effective treatment for many of these benign and malignant processes. During the past 2 decades, surgical treatment of tongue base carcinoma has been gradually supplanted by nonoperative therapy to the extent that many surgeons are unfamiliar with surgical approaches to the tongue base. This is unfortunate, as many patients in the primary and salvage treatment setting would benefit from a well-executed resection of their tongue base tumor. This manuscript is designed to elucidate the approaches involved in this endeavor.
      Regardless of diagnosis, lesions of the BOT are hard to visualize, both for the patient and the clinician. Therefore, tumors involving this region often present late in the disease process with obstructive symptoms. The most common complaints include globus pharyngeus, dysphagia, odynophagia, neck mass, referred otalgia, or hemoptysis.
      • Myers E.N.
      Operative Otolaryngology Head and Neck Surgery.
      Diagnostic workup is imperative to assess tumor extent and histology. The evaluation starts with a thorough physical examination, which includes evaluation of the neck. Flexible laryngoscopy in the seated position can provide important visual information regarding mucosal irregularities, asymmetry, and submucosal fullness within the BOT. In addition, bimanual palpation is imperative to provide tactile information regarding tumor location, submucosal extension, and, importantly, mobility of the tumor.
      • Moore E.J.
      • Janus J.
      • Kasperbauer J.
      Transoral robotic surgery of the oropharynx: clinical and anatomical considerations.
      Immobility suggests invasion into adjacent structures and may significantly alter management. It is important to also visually inspect and palpate the BOT under anesthesia to reassess location, tumor extent, and mobility, as this examination can be more sensitive than in office evaluation.
      • Moore E.J.
      • Janus J.
      • Kasperbauer J.
      Transoral robotic surgery of the oropharynx: clinical and anatomical considerations.
      Radiographic workup most commonly involves computed tomography (CT), magnetic resonance imaging, and positron emission tomography (PET) with CT, or PET/CT. CT scan can be acquired rapidly and provides information regarding primary tumor extension, bony erosion of the mandibular cortex, as well as cervical metastasis. Magnetic resonance imaging is an important adjunct for the evaluation of BOT lesions, and although more expensive and time-consuming, it gives more detailed soft-tissue information, can demonstrate submucosal tumor extension, and can help define whether transoral resection is feasible. Finally, PET/CT scans can be used to help define extent of primary disease as well as the presence of locoregional or distant metastases. Pathologic confirmation is recommended before proceeding with surgical intervention and is performed under general anesthetic either in a separate operation or just before surgical intervention under the same anesthetic.
      • Abuzeid W.M.
      • Bradford C.R.
      • Divi V.
      Transoral robotic biopsy of the tongue base: A novel paradigm in the evaluation of unknown primary tumors of the head and neck.
      Management choice depends on histopathologic diagnosis and lesion size, and can include both surgical and nonsurgical interventions, including radiation therapy and chemotherapy. We will not discuss nonsurgical interventions as they are beyond the scope of this discussion. Surgical management of the BOT presents several distinct challenges to the head and neck surgeon, and approach must be carefully weighed against the impact on functional outcome, cosmesis, and overall morbidity. With the advent of oncologically sound transoral procedures, the management of BOT pathology continues to rely heavily on surgical options. However, wide visualization and surgical access, two key components of safe oncological surgery, are often limited owing to anatomic and technical constraints. Therefore, open techniques remain an important component of surgical management. Access to the BOT can be divided into 4 basic categories: (1) transoral, (2) suprahyoid/transhyoid pharyngotomy, (3) lip-split mandibulotomy (mandibular swing), or (4) a combined “pull through” approach using intraoral incisions in addition to a visor incision. We discuss the indications, technique, and complications for each.

      Surgical approaches

      Transoral

      Indications and contraindications

      With the advent of improved instrumentation and optics, transoral approaches to this historically hard-to-reach location have increased in popularity for appropriately selected cases.
      • Henstrom D.K.
      • Moore E.J.
      • Olsen K.D.
      • et al.
      Transoral resection for squamous cell carcinoma of the base of the tongue.
      When considering the use of a transoral approach to the BOT, the surgeon must assess the size and local extension of the tumor as well as surgical access and the ability to achieve clear surgical margins. The transoral approach is ideal for T1 and T2 malignant tumors, exophytic T3 malignant disease, or benign tumors with limited extension into surrounding tissues. The most common techniques used include transoral laser microsurgery (TLM) and transoral robotic surgery (TORS). Regardless of the specific technique chosen, there are fundamental principles and limitations that can be applied to all transoral procedures. The primary advantages of this approach are the minimal invasiveness of the procedure, the ability to keep the pharyngeal musculature and neural innervation intact, the decreased tracheostomy tube and gastrostomy tube dependence postoperatively,
      • Moore E.J.
      • Olsen K.D.
      • Kasperbauer J.L.
      Transoral robotic surgery for oropharyngeal squamous cell carcinoma: a prospective study of feasibility and functional outcomes.
      the ability to keep the mandible intact, and the ease with which surgeons can proceed to open approaches when necessary.
      Moore et al and Laccourreye et al describe several contraindications to transoral approaches, which include (1) any suggestion that the tumor has invaded deeply into the adjacent parapharyngeal space, including tumor fixation to the lateral or posterior pharyngeal wall; (2) any concern for involvement of major vascular structures such as the carotid or jugular system on physical examination or imaging; (3) bony invasion into the mandible or skull base; or (4) clinically significant trismus, indicating tumor involvement of the pterygoid musculature and the potential for decreased surgical access.
      • Moore E.J.
      • Olsen K.D.
      • Kasperbauer J.L.
      Transoral robotic surgery for oropharyngeal squamous cell carcinoma: a prospective study of feasibility and functional outcomes.
      • Laccourreye O.
      • Hans S.
      • Ménard M.
      • et al.
      Transoral lateral oropharyngectomy for squamous cell carcinoma of the tonsillar region: II An analysis of the incidence, related variables, and consequences of local recurrence.
      Tumors that extend deep to the extrinsic tongue musculature (particularly the genioglossus and hyoglossus muscles) can be difficult to extirpate transorally and put the ipsilateral lingual artery, hypoglossal nerve, and carotid artery at risk. A careful assessment of clinical and radiographic data must be undertaken preoperatively to assess the relationship of the tumor to the genioglossus and hyoid bone. Involvement of, or extension beyond, these structures is a relative contraindication to transoral resection, as it places the lingual artery, hypoglossal nerve, and the external carotid artery at significant risk during resection. For any significant lateral extension, some authors recommend performing a modified or select neck dissection preemptively to identify and protect important vascular structures before performing the transoral portion of the surgical resection. Although the specific advantages and disadvantages of TLM compared with TORS are beyond the scope of this review, it is important to note that when oncological principles are followed, these techniques have resulted in relatively comparable outcomes.
      • Moore E.J.
      • Olsen K.D.
      • Kasperbauer J.L.
      Transoral robotic surgery for oropharyngeal squamous cell carcinoma: a prospective study of feasibility and functional outcomes.
      The primary disadvantages of these approaches are a limited surgical field of view (TLM more so than TORS), steep learning curve, potential for difficult hemostatic control, and cost (TORS).
      • Moore E.J.
      • Olsen K.D.
      • Kasperbauer J.L.
      Transoral robotic surgery for oropharyngeal squamous cell carcinoma: a prospective study of feasibility and functional outcomes.
      • O'Malley Jr, B.W.
      • Weinstein G.S.
      • Snyder W.
      • et al.
      Transoral robotic surgery (TORS) for base of tongue neoplasms.

      Technique

      We will discuss the fundamentals of transoral techniques and identify key differences between TLM and TORS in the following text. The procedure is performed in the operating room with the patient orally or nasally intubated with a laser-safe endotracheal tube. The teeth are protected by molded thermoplastic splints formed to guard both the maxillary and mandibular teeth. Before placement of the oral retractor, the BOT should be carefully palpated with a gloved finger to reassess tumor location, extent, and mobility, and a careful mental image of the tumor extent should be formulated by the surgeon. The tongue is retracted with a suture, if necessary, to gain deep access, and the oral retractor is then placed and suspended. Transoral approaches to the BOT depend primarily on tumor exposure, regardless of whether the surgeon is using a microscope or a robot. For TORS procedures, the Feyh–Kastenbauer retractor (Figure 1) is used most commonly, followed by the Crowe–Davis retractor, whereas for TLM procedures, the bivalved oropharyngoscope and Kleinsasser or Steiner laryngoscopes may be used. The tip of the retractor should be positioned so the anterior extent of the tumor is just visualized. If possible, exposure should also allow visualization of the inferior aspect of the tumor. This step is crucial to the overall success of the operation and may require several adjustments and trials of different mouth gags. In addition, repositioning may be necessary throughout the case, especially for large tumors, and should be considered to provide adequate exposure. Once exposure is achieved, either the operating microscope (TLM) or robot (TORS) should be brought into the field and positioned to optimize working room and field of view.
      Figure thumbnail gr1
      Figure 1Transoral approach. Setup demonstrated for transoral robotic surgery depicting the Feyh–Kastenbauer retractor. (Color version of figure is available online.)
      The choice of cutting/ablating instrument varies based on availability and surgeon preference. Electrocautery and various lasers, including carbon dioxide and thulium-doped yttrium-aluminum-garnet (Tm:YAG), can be used.
      • Van Abel K.M.
      • Moore E.J.
      • Carlson M.L.
      • et al.
      Transoral robotic surgery using the thulium:YAG laser: a prospective study.
      The first incision is made horizontally above the superior border of the tumor, which allows the tumor to “drop” into the surgical field with subsequent cuts (Figure 2). Many lateral BOT tumors invade into the tonsillar fossa and also require wide-local excision of the tonsil and superior pharyngeal constrictor muscle. The next cut is made vertically along the glossotonsillar sulcus or into the tonsillar fossa, as dictated by the tumor (Figure 3). The cut should ensure that a cuff of normal soft-tissue is removed along with the tumor specimen to provide an adequate pathologic margin of resection depending on tumor histology. The surgeon can also grasp this cuff of tissue to provide countertraction throughout the remainder of the procedure. Attention is then turned to the medial cut, which is made deep through the intrinsic tongue musculature to the level of the vallecula. This allows the surgeon to assess the depth of the tumor and provides more mobility as tangential cuts are made around the deep extent of the tumor. There are no major vessels in the midline tongue—the branches of the lingual artery enter the tongue laterally (Figure 4) —so the midline cut can be made aggressively without risk of encountering major bleeding. The tumor is slowly dissected from anterior/superior/medial to posterior/inferior/lateral until it is completely mobilized. As the surgeon approaches the lateral border, the dissection slows and blunt dissection allows identification and clipping of the dorsal lingual artery and sometimes the main lingual artery (Figure 5). In smaller tumors, en bloc resection may be possible, but for larger tumors and tumors in which the depth of invasion makes a tangential cut difficult, the tumor can be transected. Transection of the tumor allows the deepest portion to be assessed more easily, and it can also aid in visualization impaired by bulky tumors. Regardless, oncological outcomes are similar between the two techniques, and piecemeal resection should be performed if visualization and exposure are compromised by the size or position of the tumor.
      • Moore E.J.
      • Janus J.
      • Kasperbauer J.
      Transoral robotic surgery of the oropharynx: clinical and anatomical considerations.
      Figure thumbnail gr2
      Figure 2Transoral approach: the first incision is made anteriorly along the tumor margin, which, with subsequent cuts, will allow the tumor to “drop” into the surgical field. (Color version of figure is available online.)
      Figure thumbnail gr3
      Figure 3Transoral approach. Subsequent cuts are made along the lateral margins of the tumor along the glossotonsillar sulcus or into the tonsillar fossa, as dictated by the tumor. (Color version of figure is available online.)
      Figure thumbnail gr4
      Figure 4Anatomy of the base of tongue before tumor resection. Important neurovascular and muscular structures are depicted. (Color version of figure is available online.)
      Figure thumbnail gr5
      Figure 5Anatomy of the base of tongue after tumor resection. Blunt dissection allows identification and clipping of the dorsal lingual artery and sometimes the main lingual artery as the surgeon approaches the lateral border of the dissection. (Color version of figure is available online.)
      Throughout resection, the surgeon should be aware of important neurovascular anatomy and landmarks (Figure 6). The dorsal lingual artery is commonly found in the lateral tongue base and can be managed either by the primary surgeon during TLM or the assistant surgeon during TORS by placing 2 vascular clips on the patient side and 1 on the tumor side of the vessel before transection. If the vessel is cut inadvertently, pressure externally on the neck at the level of the superior thyroid cornu can slow bleeding until hemostasis can be achieved. In addition, by tracing the dorsal lingual artery laterally, the surgeon can identify the lingual artery trunk when necessary for hemostasis. During this dissection, the hypoglossal nerve may be encountered and occasionally must be resected with the surgical specimen. Although dissection may be carried across the midline, it is important to remember that if the hypoglossal nerve or lingual artery is taken on one side, the contralateral nerve or vessel must be meticulously preserved to maintain adequate function and blood flow to the oral tongue. If there is concern for lateral extension of the tumor or risk to major vasculature based on preoperative assessment or intraoperative findings, a neck dissection is recommended before transoral extirpation to identify and protect these key neurovascular structures.
      Figure thumbnail gr6
      Figure 6Vascular anatomy of the base of tongue and adjacent structures. (Color version of figure is available online.)
      A sense for pathologic versus normal tissue response to the cutting/ablating tool being used for dissection in the BOT is important, as margins are often difficult to assess visually during resection and tactile feedback may be limited depending on surgical approach used. For example, some authors report that normal tissue separates easily with the spatula-tipped cautery during TORS, whereas keratinized tumor separates more slowly.
      • Moore E.J.
      • Janus J.
      • Kasperbauer J.
      Transoral robotic surgery of the oropharynx: clinical and anatomical considerations.
      Maximizing the optical benefit of either the microscope or endoscope is also important to help visually assess tumor margins. These considerations underscore the importance of frozen-section analysis and an integrated system for personal communication between surgeon and pathologist. Once the tumor is completely freed, it is removed from the oropharynx and oriented by the surgeon. The margins of resection are inspected, and the tumor is “walked” to the pathologist by the surgeon so that direct verbal communication and tumor inspection by both parties can ensure precise assessment of the surgical margins. Based on feedback from the pathologist, additional surgical margins may be required. These must be carefully oriented and discussed with the pathologist to ensure adequate resection. Once negative margins are achieved, the wound is copiously irrigated with sterile saline and hemostasis is ensured. Most commonly, the wound is left to heal by secondary intention. In almost all cases, a nasogastric feeding tube is placed, which can be removed shortly postoperatively, as the patient demonstrates adequate swallow function.
      At this juncture, attention is turned to the neck. Ipsilateral or bilateral select neck dissections are performed as dictated by the tumor and the surgeon preferences. During dissection, the senior author recommends ligation of the ipsilateral facial and lingual arteries to decrease the risk of postoperative hemorrhage. After completion of cervical dissection, the nares are occluded and the oral cavity is vigorously flooded with sterile saline while the areas at risk for communication in the neck are observed for a leak. If identified, this is addressed by oversewing the constrictor musculature either transorally or through the neck. At our institution, we close a portion of the digastric muscle to the sternocleidomastoid muscle lateral to the defect. We then apply a layer of Tisseel (Baxter Bioscience, Deerfield, IL) over the defect in the neck. If a communication was encountered and closed, a nasogastric feeding tube should be placed. After careful closure of the neck incisions over suction drains, the surgeon should again evaluate the oropharynx to assess edema and safety of extubation. Depending on examination findings, the patient can be extubated, undergo tracheostomy, or be transferred to an intensive care unit for delayed extubation. Once the airway is secure, the patient is taken to the postanesthesia care unit for recovery.

      Complications

      Complications associated with transoral resection of BOT lesions can be divided into minor and major categories. Minor complications include altered taste, chipped teeth, odynophagia, trismus, dysphagia, and otalgia. Although many of these complications are anticipated, their occurrence may be minimized by taking care to preserve uninvolved neurovascular structures and choosing instruments that decrease injury to adjacent normal tissue. Major complications include postoperative intraoral hemorrhage, hematoma, airway compromise, urgent or emergent tracheostomy, and aspiration pneumonia. The risk of perioperative death is rarely reported in current series and may be minimized by appropriately selecting surgical patients.
      • Henstrom D.K.
      • Moore E.J.
      • Olsen K.D.
      • et al.
      Transoral resection for squamous cell carcinoma of the base of the tongue.
      • Moore E.J.
      • Olsen K.D.
      • Kasperbauer J.L.
      Transoral robotic surgery for oropharyngeal squamous cell carcinoma: a prospective study of feasibility and functional outcomes.
      • O'Malley Jr, B.W.
      • Weinstein G.S.
      • Snyder W.
      • et al.
      Transoral robotic surgery (TORS) for base of tongue neoplasms.
      Although rare, the occurrence of life-threatening oropharyngeal hemorrhage in the postoperative period has been reported. The senior author recommends identifying and ligating the ipsilateral facial and lingual arteries during neck dissection to decrease this risk. In addition, taking care to identify and properly clip the dorsal lingual artery transorally is important. The development of hematomas may be avoided by meticulous hemostasis; however, even the most careful surgeon may experience this complication. Recommended management involves return to the operating room for evacuation of the blood clot and hemostasis, although bleeding vessels are rarely found. Unplanned tracheostomy can be limited by carefully examining the patient after surgical resection and performing planned tracheostomy or delaying extubation to allow abatement of the associated edema. One of the reported benefits of transoral resection of BOT tumors is the low tracheostomy and gastrostomy tube dependence rates reported in the literature.
      • Moore E.J.
      • Olsen K.D.
      • Kasperbauer J.L.
      Transoral robotic surgery for oropharyngeal squamous cell carcinoma: a prospective study of feasibility and functional outcomes.
      • Laccourreye O.
      • Hans S.
      • Ménard M.
      • et al.
      Transoral lateral oropharyngectomy for squamous cell carcinoma of the tonsillar region: II An analysis of the incidence, related variables, and consequences of local recurrence.
      Despite this, oropharyngeal dysphagia and aspiration are serious concerns. We recommend performing a formal swallow study by a trained speech therapist (either bedside or under video fluoroscopy) before allowing an oral diet for those patients at risk, as dictated by intraoperative findings and individual functional status. Finally, orocutaneous fistulas are reported in patients undergoing concomitant neck dissection. Although persistent fistula is rare, prompt recognition and management by placing a feeding tube, eliminating oral intake, and performing local wound cares can prevent acute complications and long-term functional debility.
      • Moore E.J.
      • Olsen K.D.
      • Martin E.J.
      Concurrent neck dissection and transoral robotic surgery.

      Suprahyoid (transhyoid) pharyngotomy

      Indications and contraindications

      The suprahyoid pharyngotomy offers an open midline approach to the BOT, which is best suited for midline lesions and benign tumors or low-grade salivary gland tumors of the BOT. In addition, this approach can be used for T1 or T2 malignant lesions that are inaccessible transorally, radioresistant, or have failed nonoperative therapy. It can also be used for larger lesions not conducive to transoral approaches, and can be extended into a lateral pharyngotomy to allow resection of tumors with more extensive involvement of the oropharynx, hypopharynx, or larynx. However, most authors recommend this approach for BOT tumors with minimal extension beyond the tongue base. In his report on suprahyoid pharyngotomy in 1991, Zeitels
      • Zeitels S.M.
      • Vaughan C.W.
      • Ruh S.
      Suprahyoid pharyngotomy for oropharynx cancer including the tongue base.
      specifically reported that this approach afforded excellent exposure of BOT lesions that do not involve the mandible or vallecula. Suprahyoid pharyngotomy therefore offers an open surgical approach with excellent exposure of the BOT without the sequelae of mandibulotomy.
      This approach is relatively contraindicated for lesions that extend beyond the BOT or involve adjacent structures, such as the vallecula, the lingual surface of the epiglottis, or the mandible. In addition, if there is tumor extension anterior to the circumvallate papillae, this approach is relatively contraindicated owing to difficult visualization and wound closure. Lesions should not involve both lingual arteries, as resection of both vessels will result in the need for total glossectomy. The disadvantage of this approach is the frequent need for tracheostomy, although this is somewhat debatable.
      • Zeitels S.M.
      • Vaughan C.W.
      • Ruh S.
      Suprahyoid pharyngotomy for oropharynx cancer including the tongue base.
      In addition, there is the potential for an increased risk for pharyngocutaneous fistula owing to the nature of the procedure; however, this risk can be minimized with careful surgical closure.

      Technique

      The procedure is performed in the operating room under general anesthesia. Most surgeons recommend a planned tracheostomy at the start of the procedure to eliminate the interference of an oral or a nasal endotracheal tube within the operative field. Before prepping the patient, the BOT should be carefully palpated with a gloved finger to reassess tumor location, extent, and mobility, keeping in mind the point of entry for pharyngotomy. The patient is then prepped and draped, maintaining access to the oral cavity. Draping in this way allows an assistant to place a finger or retractor into the oral cavity at a later point during the procedure in the event this is required.
      A superiorly based incision is created in a submental skin crease, which can be extended into the submandibular area for neck dissection. This incision should allow direct access to the hyoid bone. When indicated, ipsilateral or bilateral neck dissections should be performed before pharyngotomy. At our institution, a select neck dissection including levels I–IV and submandibular gland excision are performed for BOT tumors. Care should be taken to identify the hypoglossal nerves, superior laryngeal nerves, and lingual arteries bilaterally and to preserve them whenever possible. These vessels can be tagged with vessel loops to assist in preservation. The ipsilateral lingual and facial arteries do not need to be ligated and transected to decrease the risk of postoperative hemorrhage if the intraoral wound is being closed primarily (Figure 6). The hyoid bone and suprahyoid musculature are then carefully defined, and electrocautery is used to dissect the muscles from their origin at the hyoid. A 5-mm cuff of muscle can be left on the hyoid hone to facilitate closure or the muscles can be sharply divided at the bone. The hyoid bone can be grasped with an Allis clamp or tenaculum and retracted in an anterior and inferior direction to provide exposure and countertraction. The pre-epiglottic space is then exposed and the hyoepiglottic ligament is defined using gentle blunt dissection to divide the suprahyoid and intrinsic tongue musculature from this key landmark. At this juncture, a condensation of fibers can be visualized in the midline as the glossoepiglottic fold, which provides attachment for the epiglottic mucosa. Again, this loose mucosa can be elevated completely off the lingual surface of the epiglottis with gentle blunt dissection. The hyoepiglottic ligament then offers a key landmark, as its broad hyoid origin leads to a tapered insertion into the tip of the epiglottis, directing the surgeon to a relatively safe point of entry into the pharynx. A pharyngotomy is then made by grasping the mucosa just superior to the insertion of this ligament and using a Metzenbaum scissor (or similar) to sharply enter the pharynx. A broad right-angled retractor can then be inserted above the tongue base to provide countertraction to that exerted on the hyoid bone while the pharyngotomy is completed, taking care to avoid violating the lesion of interest (Figure 7). Throughout this portion of the procedure, it is important to keep the hypoglossal nerve, lingual artery, and superior thyroid neurovascular bundle in mind to prevent inadvertent injury.
      Figure thumbnail gr7
      Figure 7Suprahyoid pharyngotomy approach. The surgeon approaches the pharyngotomy through a suprahyoid incision, leaving a cuff of muscle along the hyoid bone for closure (large window). The point of entry is at the hyoepiglottic ligament. After entry, the tumor is evaluated and a tenaculum or Allis clamp can be placed on the BOT to draw it out through the pharyngotomy (small window). (Color version of figure is available online.)
      Once the pharyngotomy is complete, a tenaculum or Allis clamp can be placed on the BOT to draw it out through the pharyngotomy (Figure 8). This provides direct visualization of the BOT lesion, allowing for complete resection with an adequate margin of healthy tissue. A small Deaver retractor can then be inserted into the oral cavity to assist in holding the BOT in place during resection of the primary tumor. If additional exposure is required, the central portion of the hyoid bone can be excised. Despite improved visualization and tactile feedback, it may difficult to predict margin status for some tumors. It is therefore important to orient the specimen correctly and communicate personally with the pathologist performing frozen-section analysis to obtain adequate margin status. If additional margins are necessary, they should be completed at this time. Once negative margins are obtained, a nasogastric tube should be inserted for postoperative nutrition. The wound is then closed primarily by suturing the BOT mucosa to the vallecular mucosa. A second layer closes the intrinsic musculature and suprahyoid musculature to the hyoid periosteum or remaining muscular cuff. After completion of cervical dissection, the nares are occluded and the oral cavity is vigorously flooded with sterile saline while the areas at risk for communication in the neck are observed for a leak. If identified, these areas are reinforced by oversewing muscle and reassessing. Tisseel (Baxter Bioscience, Deerfield, IL) can then be applied. Finally, a multilayered skin closure should be performed over suction drains placed in the neck. If a tracheostomy was not performed initially, it can be performed at the end of the procedure, if indicated. The patient is then awakened and taken to the postanesthesia care unit for recovery.
      Figure thumbnail gr8
      Figure 8Cervical incision for lip-split mandibulotomy approach. Horizontal incision may be used for unilateral or bilateral neck dissections. The vertical incision is used for lip-split mandibulotomy or mandibular swing procedures. The vertical portion should be divided into several geometrical angles to prevent contracture. (Color version of figure is available online.)

      Complications

      Complications associated with suprahyoid/transhyoid pharyngotomy are similar to those described for transoral tumor resection (see above). The risk of oropharyngeal hemorrhage is lessened because the wound is closed primarily. One important complication is underestimating the size of the tumor with respect to anterior or lateral extension. Unexpected anterior extension could necessitate total glossectomy and subsequent severe aspiration, requiring additional intervention such as completion laryngectomy. However, Weber et al
      • Weber P.C.
      • Johnson J.T.
      • Myers E.N.
      The suprahyoid approach for squamous cell carcinoma of the base of the tongue.
      report that the use of suprahyoid pharyngotomy may help minimize understaging of tumors, and when understaging does occur, the flexibility afforded by this approach can accommodate resection of a larger/more extensive tumor.

      Lip-split mandibulotomy (mandibular swing)

      Indications and contraindications

      The lip-split mandibulotomy (mandibular swing) approach gives wide access to the posterior oropharynx and supraglottis. This approach is indicated in patients with severe trismus, complicated anatomy, deeply invasive tumors, and tumors that are intimately related to the carotid vasculature. Lip-split mandibulotomy allows the surgeon to appreciate the extent of the tumor by palpation as well as visualization, allows excellent access to the vasculature of the head and neck for control of bleeding, and allows the surgeon wide access to the surgical defect for placement of reconstructive flaps. Mandibulotomy approaches often require soft-tissue reconstruction of the pharynx for closure, and the surgeon must pay careful attention to dentition and occlusion during creation and closure of the mandibulotomy. Although most patients recover without significant cosmetic deformity, this procedure is largely contraindicated in patients who are concerned with cosmetic outcome. In addition, mandibulotomy is not recommended for those patients with poor wound healing owing to risk of wound breakdown, infection, and mandibular nonunion. These clinical conditions can include uncontrolled diabetes, a history of radiation therapy, or immunosuppression. In addition, this procedure should be reserved for cases that need wide exposure, and therefore, it is not suitable for small BOT lesions that are accessible through less-invasive techniques.

      Technique

      The operation requires placement of a tracheostomy, which is usually performed at the beginning of the operation to allow unencumbered visualization and access to the surgical field. If the tumor obstructs clear visualization of the airway, the tracheostomy is placed with the patient awake under local anesthesia; otherwise the patient can be intubated with subsequent tracheostomy under general anesthesia. A horizontal incision is made across the mid neck ipsilateral to the tumor or directly across both sides of the neck if bilateral neck dissections are to be performed (Figure 8). Subplatysmal flaps are raised up to the mandible and down to the clavicle(s). Ipsilateral or bilateral neck dissection is then performed, as indicated, before proceeding to mandibulotomy. Our preference is to perform bilateral neck dissections for patients with extensive BOT tumors. Dissection of level I of the neck on the side of the tumor and skeletonization of the digastric muscle, mylohyoid muscle, lingual and hypoglossal nerves, and lingual artery on this side facilitate the mandibulotomy approach. The ipsilateral lingual artery is ligated in the neck. It is imperative to preserve the contralateral lingual artery and hypoglossal nerve if the patient is to maintain speech and swallowing function postoperatively.
      The mandibulotomy approach is begun by extending the cervical incision vertically through the upper neck flap in the midline through the submental skin to the submental crease (Figure 9). The incision is then extended around the mentum to the supramental crease, and then superiorly to the vermillion–cutaneous junction of the lip. Some surgeons prefer the cosmetic appearance of an incision directly through the midline of the chin—either approach is acceptable. Regardless, the scar will be improved by breaking the vertical portion into several geometrical angles to prevent contracture. Marking the vermillion–cutaneous juncture with methylene blue tattooing before incision will facilitate reapproximation at the time of closure. The incision is carried through the mucosa and orbicularis muscle, and the inferior labial artery is ligated or bipolar cauterized. The incision is then carried 1-2 cm along the gingival buccal sulcus to expose 1.5 cm of ipsilateral mandible on the side of the tumor, taking care to preserve enough mucosal tissue along the mandible to facilitate mucosal closure at the end of the procedure without dissecting so far laterally as to transect the mental nerve (Figure 9). The anterior digastric muscle and mylohyoid muscle are then dissected off the mandible on the side of the tumor, and blunt dissection is carried along the lingual surface of the mandible and through the floor of mouth mucosa to allow placement of a malleable elevator in this area at the time of the mandibular cuts. A stair-stepped mandibulotomy is outlined on the mandible lateral to the symphysis and medial to the mental foramen. A lateral incisor tooth can be removed to facilitate the alveolar cut, or the cut can pass between the teeth if there is adequate space for the sagittal saw blade. The length of the cuts is approximately 1 cm, and an appropriate width saw blade should be chosen. To maintain proper mandibular alignment and occlusion, a 2.0 locking mandibular plate is placed along the inferior border of the mandible with at least 2 bicortical screws on either side of the inferior mandibulotomy cut. A smaller plate with monocortical screws is placed along the superior mandibulotomy cut. The plates should be placed and the holes drilled initially. The plates are then removed, oriented, and set aside for use at the time of closure. If the patient is edentulous, plates do not need to be predrilled before the mandibulotomy. With the malleable retractor protecting the soft-tissue on the lingual surface of the mandible, a sagittal saw is used to perform the stair-stepped mandibulotomy cuts completely through the mandible. Continuous irrigation should be used during the saw cuts to protect the bone from heat damage. After the mandible is cut completely, the edges will separate enough to place a bone hook retractor on the lateral mandibular edge. Electrocautery is then used to create a mucosal soft-tissue cut (with completion of mylohyoid and medial pterygoid muscle cuts) on the lingual surface of the mandible up to retromolar trigone and, if necessary, through the anterior tonsillar pillar or into the tonsillar fossa. Again, care should be taken to preserve a cuff of mucosa on the lingual surface of the mandible to facilitate closure.
      Figure thumbnail gr9
      Figure 9Mandibulotomy. Demonstration of the important neurovascular, bony, and muscular structures exposed through mandibulotomy. Note the stair-step bony cuts. The tumor is carefully identified and dissected around. (Color version of figure is available online.)
      The tongue and floor of mouth tissue are left attached to the medial mandible. Retraction on the tongue now allows excellent visual inspection and palpation of the BOT and oropharyngeal lesion. The lingual nerve can be left intact, or severed if it impedes access to the tumor. The lingual artery should be ligated for ipsilateral BOT resection to facilitate tumor dissection and decrease postoperative bleeding. The hypoglossal nerve can be preserved or transected, as dictated by intraoperative findings. The tumor resection proceeds with an unguarded blade tip cautery through the intrinsic and extrinsic tongue musculature, into the pharynx or supraglottis, as necessary. The surgeon should take care to resect an adequate margin of normal tissue around the tumor for margin analysis by the pathologist. Frozen-section pathology can greatly facilitate complete BOT tumor removal. Resection of a substantial portion of the BOT and supraglottic larynx results in significant aspiration in most patients, and consideration should be given to total laryngectomy in patients who lose more than three-quarters of the BOT, have accompanying supraglottic larynx and tongue base involvement, or who are predicted to poorly tolerate aspiration secondary to their medical comorbidities.
      After complete cancer removal, as confirmed by margin analysis, reconstruction and closure can commence. The tongue surface and neck are irrigated with saline and inspected for bleeding, a feeding tube is placed transnasally into the stomach, and the defect is measured and reconstructed with a soft-tissue pedicled or vascularized flap, as necessary. Reconstruction of the pharyngeal and tongue base defect is usually necessary to allow fistula-free healing and return to swallowing. Closure is completed by closing the entire soft-tissue defect in a watertight fashion with resorbable mattress sutures, closing the mandibulotomy with the previously fashioned and bent reconstruction plates, and closing the lip wound meticulously with mucosal, muscle, and skin stitches. The neck wounds are closed over suction drains, and the endotracheal tube is changed to a cuffed tracheostomy and sutured to the neck skin.

      Complications

      Mandibulotomy commonly involves perioperative edema and prolonged healing time that can delay return to speech and swallowing for several weeks. Complications of mandibulotomy include cosmetic defects of the skin of the neck, lip, and chin. These can be minimized with meticulous closure technique, careful approximation of the orbicularis muscle and vermillion–cutaneous junction, and appropriate choice of suture. Patients are frequently worried about the cosmesis of the procedure when told about division of the lip and mandible, but cosmetic results, particularly in the patient with more pronounced facial rhytids, are commonly acceptable. Malocclusion, loss of dentition, and mastication problems can occur. The incidence of these can be minimized with careful operative planning, execution, and careful plating of the mandibulotomy defect. Mandibulotomy coupled with postoperative radiotherapy can result in malunion of the mandibulotomy site, hardware exposure, and osteonecrosis around the mandibulotomy site. These are the most troublesome complications of mandibulotomy, and can occur years after the procedure. Sometimes these occurrences require hardware removal or replacement, or even mandibular vascularized reconstruction. Because these bony complications can be difficult to repair, some surgeons avoid the approach, and substitute transoral resection or transhyoid pharyngotomy to prevent devascularization of the mandible. A compromise that will allow adequate exposure without sacrificing the mandible is the pull-through technique.

      Pull-through technique with visor incision

      Indications and contraindications

      The pull-through technique is indicated for large tumors of the BOT when the surgeon needs wide exposure but does not want to split the mandible or lip. The visor incision can be cosmetically preferable to the lip-split incision, and may be preferable in younger patients or patients with high cosmetic demands who require extensive BOT surgery. Partial pull-through can be performed for unilateral resections, whereas bilateral pull-through can be performed for larger tumors that cross the midline or when total glossectomy is to be performed. The technique is not indicated for smaller tumors when transoral resection or pharyngotomy will suffice, or when the patient is not tolerant of tracheostomy placement.

      Technique

      As in the mandibulotomy approach, the procedure is initiated with tracheostomy, followed by a bilateral horizontal mid neck incision, ideally placed in a horizontal neck rhytid (Figure 8). The superior flap is raised in the subplatysmal plane up to the submandibular level. The marginal mandibular nerves are identified bilaterally; the facial arteries and veins are divided beneath the mandibular notches. The flaps are then raised deep to the marginal nerves and superior vessels above the mandibular border (Figure 10). After neck dissections are performed, the patient is paralyzed to allow easier mouth opening. The mylohyoid and digastric muscles are released from the mandible, followed by the genioglossus muscles. Intraoral mucosal cuts are then performed transorally with cautery along the lingual surface of the mandible, taking care to preserve a mucosal cuff of tissue along the inner surface of the mandible to allow for closure. Continuing the cuts up to the retromolar trigone and into the tonsillar fossa and pharynx allows for enough mobility of the tongue so that it can be dropped beneath the mandible and visualized in the neck (Figure 11). The surgeon can then proceed with tumor removal by making cautery cuts through the tongue mucosa, intrinsic muscles, and extrinsic muscles, as necessary. The tumor should be kept in view and be available for palpation during extirpation to prevent violation. As with other tongue resections, generous margins of normal tissue confirmed by frozen-section pathology ensure complete tumor extirpation.
      Figure thumbnail gr10
      Figure 10Visor flap. The superior flap is raised in the subplatysmal plane up to the submandibular level. Intraoral mucosal cuts are then performed transorally with cautery along the lingual surface of the mandible (hatched line). (Color version of figure is available online.)
      Figure thumbnail gr11
      Figure 11Pull-through technique. Continuing the cuts up to the retromolar trigone and into the tonsillar fossa and pharynx allows for enough mobility of the tongue so that it can be dropped beneath the mandible and visualized in the neck. (Color version of figure is available online.)
      After tumor removal, begin closure by first thoroughly irrigating the tongue surface and neck and ensuring hemostasis. A nasogastric feeding tube should be placed and the tongue returned to its native position. A watertight closure of the mucosal edges by meticulous placement of resorbable mattress sutures is performed. The mouth is then irrigated with inspection of the neck to assess for leak, and any leaks are repaired either with transoral or transcervical placement of sutures. Closure with a soft-tissue flap may be necessary, depending on the extent of resection. The genioglossus and mylohyoid muscles may be reapproximated, and then the neck is closed over suction drains and a cuffed tracheostomy tube is placed.

      Complications

      The tongue pull-through technique can be associated with fistula formation. However, meticulous preservation of mucosal tissue, atraumatic and meticulous technique of resection, and careful closure can help prevent this. In patients who have been previously treated, are malnourished, or have severe comorbidities, delayed healing and mandible exposure can occur, requiring soft-tissue vascularized flaps for reconstruction.
      Dysarthria and dysphagia can also occur. Preservation of 1 lingual arteries and 1 hypoglossal nerve is essential, and preservation of both hypoglossal nerves and lingual arteries is preferable, to maximize speech and swallowing function. However, oncological resection should never be compromised for this purpose. Ranulas can also occur after the pull-through procedure. This complication can be minimized by removal of the sublingual glands and submandibular glands ipsilateral to the tumor and more extensive surgical resection.

      Discussion

      The tongue base provides a significant challenge to the head and neck surgeon in terms of visualization and access. However, there are multiple procedures available to provide surgical exposure and oncological resection while minimizing overall morbidity. With the advent of new instrumentation and optics, transoral access to the BOT is now not only feasible, it is relatively commonplace. In addition, several studies have shown that transoral surgical resection results in decreased morbidity when compared with open techniques.
      • Henstrom D.K.
      • Moore E.J.
      • Olsen K.D.
      • et al.
      Transoral resection for squamous cell carcinoma of the base of the tongue.
      • Moore E.J.
      • Olsen K.D.
      • Kasperbauer J.L.
      Transoral robotic surgery for oropharyngeal squamous cell carcinoma: a prospective study of feasibility and functional outcomes.
      • O'Malley Jr, B.W.
      • Weinstein G.S.
      • Snyder W.
      • et al.
      Transoral robotic surgery (TORS) for base of tongue neoplasms.
      Despite these advances, transoral access is not appropriate for certain tumors. For BOT lesions not amenable to transoral resection, suprahyoid pharyngotomy, mandibular swing, and pull-through procedures offer a range of interventions that provide the surgeon increasingly wider access to larger more complex tumors.
      Regardless of the technique chosen, the primary goals of the surgery are to achieve negative tumor margins without compromising form or function, or increasing patient morbidity. It is important to note that for each of the procedures described herein, reconstruction may impact these secondary goals. Reconstruction may consist of leaving the wound open to heal by secondary intention, as in most transoral procedures; primary closure, as in suprahyoid pharyngotomy; a local flap or free tissue transfer, seen for the more extensive open procedures. Although detailed discussion of oropharyngeal reconstruction is beyond the scope of this article, some mention is warranted owing to the significant impact reconstruction can have on the functional outcome for each procedure. Henstrom et al
      • Henstrom D.K.
      • Moore E.J.
      • Olsen K.D.
      • et al.
      Transoral resection for squamous cell carcinoma of the base of the tongue.
      argue that for transoral resection, healing by secondary intention may result in a contracted wound site that when covered by mucosalized tissue may function better in both speech and swallow than a large, bulky, insensate tissue flap. However, when a large defect is required for adequate tumor resection, Sabri et al
      • Sabri A.
      Oropharyngeal reconstruction: current state of the art.
      note that surgeons are now able to provide good function and improved quality of life with advances in oropharyngeal free flap reconstruction.
      Although the BOT has been challenging to surgeons throughout history, it has also provided a unique stimulus for research and innovation. Development of TLM and TORS was both fostered in part by the desire to address BOT tumors transorally and minimize patient morbidity. Suprahyoid pharyngotomy was applied to BOT lesions that were inaccessible transorally, but did not require mandibulotomy or laryngectomy for adequate oncological resection. Finally, mandibular swing and pull-through procedures provided the needed surgical access for complex BOT lesions that require extensive resection. Interestingly, these procedures can be considered on a treatment continuum, allowing each unique tumor to be treated with an individualized approach. The head and neck surgeon must therefore be facile in each technique, understand the advantages and disadvantages, and be able to adjust surgical plans based on intraoperative findings without sacrificing oncological or functional goals.

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