63: Subglottic Resection of the Airway

The use of cricotracheal resection in the treatment of cancer is rare owing to the rarity of cancers of the subglottis and their lack of confinement to the larynx. Of the three subsites of the larynx, the subglottis is the origin of squamous cell carcinoma (by far the most common cause of laryngeal cancer), in only 1% to 3% of patients.¹ Cricotracheal resection for the treatment of subglottic stenosis is much more common, and the surgical techniques used for treating subglottic stenosis can be applied to surgical resection of the rare neoplasm that remains confined to the subglottis.

The glottis is defined by the American Joint Committee on Cancer as the superior and inferior surfaces of the true vocal cords occupying a horizontal plane 1 cm in thickness extending inferiorly from the lateral margin of the ventricle, including the anterior and posterior commissures. The subglottis is defined as that region which extends from the lower border of the glottis to the lower margin of the cricoid cartilage.² On the basis of histologic sectioning of whole larynges, Kirschner³ was able to demonstrate that the conus elasticus represents the definitive anatomic boundary between the glottis and the subglottis. Tumors above the plane of the conus elasticus tend to behave as glottic tumors and remain within the confines of the larynx, whereas those below the conus spread more easily beyond the borders of the larynx and metastasize more commonly to the prelaryngeal, paratracheal, and mediastinal lymph nodes.^1,4 The epithelial lining also can be used to differentiate the glottis (lined by keratinizing squamous cells) from the subglottis (lined by ciliated respiratory epithelium).

Although squamous cell carcinoma arises in the subglottis in only 1% to 3% of all laryngeal cancers, the subglottis is involved by contiguous spread of tumors of glottic origin in 11% to 33% of patients. These more common tumors are not amenable to cricotracheal resection.⁵ Early primary subglottic carcinomas are asymptomatic. Patients generally present with stage T3 or T4 tumors (Table 63-1), and airway obstruction is relatively common. These tumors usually exhibit circumferential growth, early cartilage invasion, and tumor growth beyond the borders of the larynx. Since glottic tumors with subglottic extension are not amenable to cricotracheal resection, and primary tumors of the subglottis of grade T2 or above are not contained within the subglottis, cricotracheal resection for squamous cell carcinoma is only possible for the rare T1 tumor. Otherwise, subglottic squamous cell carcinoma is treated with either radiation therapy or wide-field surgery, such as laryngectomy or laryngopharyngectomy. Tracheal tumors rarely extend superiorly to involve the subglottis. There is also strong evidence that subglottic squamous cell carcinomas should be treated aggressively, as there are poor outcomes published with advanced disease, and there is a propensity for nodal and distant metastasis.¹

Unlike the glottis, the subglottis contains laryngeal mucous glands and can be the primary site of tumors that arise from these glands. Nonsquamous laryngeal carcinomas make up only 1% to 5% of laryngeal cancers. They consist of adenocarcinoma, adenoid cystic carcinoma, mucoepidermoid carcinoma, neuroendocrine tumors, and cartilaginous tumors. In addition, plasmacytomas, non-Hodgkin lymphoma, and metastatic lesions can arise in the subglottis. Although different tumors require varying margins of resection and may respond to radiation with different efficacies, the selected early nonsquamous cell carcinoma may be resected by cricotracheal resection if the correct conditions exist. Perhaps best suited for cricotracheal resection is the chondroma or chondrosarcoma, the most common laryngeal sarcoma, representing 1% of all laryngeal tumors.⁶ Because the low-grade form of chondrosarcoma is easily confused with the benign chondroma, the true incidence is difficult to know. Chondrosarcomas arise from the hyaline cartilages of the larynx, and most commonly arise from the cricoid (70%), especially the posterior lamina, followed by the thyroid cartilage (20%), and the arytenoids (10%).⁷ Endoscopically, chondrosarcomas of the posterior cricoid lamina tend to grow into the airway, causing obstruction, and rarely, they extend beyond the confines of the perichondrium. As a consequence of the unresponsiveness of low-grade chondrosarcomas to radiation therapy and their confined growth patterns, cricotracheal resection with voice preservation can be accomplished.⁸ This often occurs after multiple endoscopic resections have failed to ameliorate the recurring airway obstruction. Paragangliomas and granular cell tumors of the subglottis are also amenable to cricotracheal resection.

Laryngotracheal invasion by thyroid carcinoma has an incidence of 7%.⁹ Invasion of the thyroid and cricoid cartilages occurs through direct extension and represents a rare but important cause of death from well-differentiated thyroid carcinoma. Controversy exists over the treatment of locally invasive thyroid carcinoma. “Shaving” the tumor from the larynx and trachea, followed by treatment with ¹³¹I, produces good long-term control of the disease, but this technique is only effective if no gross residual tumor is left behind.¹⁰

Subglottic and superior tracheal stenoses remain the most common indications for cricotracheal resection, and the principles of this technique are easily applied to surgical resection of the rare amenable neoplasm. Mechanical ventilation from endotracheal intubation remains the most common etiology of laryngeal stenosis.¹¹ Mucosal injury by either the tube or the balloon cuff results in either ischemia from pressure or mucosal tears from movement or placement of the tube. These iatrogenic events can lead to mucosal ulceration, perichondritis, chondritis, and finally, cartilage necrosis. The injury can occur at the glottic, subglottic, or tracheal levels and is largely preventable by early tracheotomy and aggressive adjunctive management, such as antibiotics and proton pump inhibitors. Laryngotracheal stenosis can also be caused by autoimmune diseases, infection, scar formation post tracheotomy, and idiopathic causes. Subglottic stenosis can be found in 16% to 20% of patients with Wegner's granulomatosis.¹² In our own practice, having treated more than 80 patients with Wegner's granulomatosis and subglottic stenosis, we find that endoscopic treatment of the stenosis, including direct injection of steroid and balloon dilation has prevented the necessity of tracheotomy or open airway reconstruction in all patients.¹³ In previously treated patients, especially in those who have undergone multiple endoscopic laser excisions, we have had to resort to open laryngotracheal reconstruction.

Tracheal and subglottic damage is often due to tracheotomy tube injuries. Inappropriately high tracheotomies, migration of the tube superiorly, and suprastomal granulation tissue are common causes of failure to decannulate patients after tracheotomy.¹⁴ The cause of the superior migration is unknown but may be due to movement from swallowing or external neckties that pull the tube superiorly. These patients often are amenable to cricotracheal resection but are challenged by extensive damage of the trachea and cricoid from chronic infection caused by microbial colonization of the tracheotomy tube, in addition to the concurrent disease that necessitated the tracheotomy in the first place. Contraindications in our own practice for cricotracheal resection for tracheotomy removal include poorly controlled diabetes, systemic steroid therapy, likely need for intubation in the near future, obstructive sleep apnea, and concomitant pulmonary disease. Similarly, poorly controlled diabetes, systemic steroid therapy, and severe pulmonary disease are contraindications to cricotracheal resection for neoplasms of the subglottis, and nonsurgical treatments such as radiation therapy, chemotherapy, and palliative therapy are best suited to patients with significant comorbidities.

Office assessment of the patient includes flexible nasal fiberoptic endoscopy to exclude glottic involvement, vocal fold fixation and posterior commissural interarytenoid stenosis, and impending airway compromise. Fine-cut CT scan determines cartilage invasion and extralaryngeal spread, as well as cervical lymphadenopathy. Three-dimensional reconstruction and “fly through” radiologic endoscopy can further define the pathologic process. It is our practice to use full-body CT/PET to exclude regional and distant disease. Combined endoscopy under general anesthesia including direct laryngoscopy with biopsy, bronchoscopy, and esophagoscopy permit tissue diagnosis, debulking, determination of the inferior extent of the tumor, and exclusion of esophageal spread posteriorly. Patients should be warned that their voice will be hoarse for some period postoperatively and that the quality of their voice may differ permanently with a decrease of fundamental frequency of approximately 10 Hz. This effect can be even more pronounced in women as shown by Smith et al.¹⁵ with a mean decrease in fundamental frequency of 21 Hz in the 14 women they evaluated having undergone cricotracheal resection. The reason for this decrease in fundamental frequency is that the cricothyroid muscle is resected at its attachment to the anterior cricoid ring, resulting in an inability to tense the vocal fold which is the normal physiologic function of the cricothyroid muscle.

Figure 63-1 demonstrates the common technique of cricotracheal resection for circumferential subglottic stenosis. This technique is described not only for use by surgeons wishing to resect stenoses but also for those wishing to excise tumors of the subglottis, as demonstrated in Figure 63-2. In most cases of subglottic tumor resection, the mucosa and submucosa overlying the posterior plate of the cricoid needs to be resected. In some amenable tumors, partial vertical height of the cricoid must be resected to obtain suitable margins, preserving enough posterior cricoid cartilage superiorly and between the arytenoids to preserve arytenoid stability. If the mucosa is resected up to the interarytenoid area, or if a limited margin exists inferior to the true vocal fold, laterally hindering normal vocal fold movement, a laryngofissure is created not only to permit adequate exposure but also to incorporate the use of a stenting T-tube around which healing occurs, preventing postoperative glottic stenosis (Fig. 63-3).

Stenosis Resection

Figure 63-1 demonstrates the common appearance of circumferential subglottic stenosis with involvement of the upper tracheal rings. Not only is the anterior subglottis narrowed, but also the posterior thickening impedes airway patency. Resection of such lesions is begun with induction of anesthesia by transoral intubation with a small-caliber endotracheal tube, often of an extended length to permit later entrance into the trachea without violating the balloon cuff. If the stenosis is of such caliber that dilation must take place before intubation, jet ventilation is used temporarily during the dilation, which is minimal, to avoid causing too much edema. A previously existing tracheotomy tube can be used for induction but is changed immediately to translaryngeal intubation such that the tracheostomy tube does not crowd the operative field. After intubation, the head is extended with a shoulder roll, and a transverse incision is made from sternocleidomastoid to sternocleidomastoid superior to the manubrium. The skin flaps are raised subplatysmally superiorly to the hyoid bone and inferiorly to the clavicles. The strap muscles are separated, and the thyroid gland is divided at the isthmus. Neither suprahyoid nor thyrohyoid release maneuvers are routinely used. The trachea is dissected in a pretracheal plane, very close to the cartilaginous rings to avoid damaging the recurrent laryngeal nerves, which we do not identify routinely. The trachea is dissected down to the carina to produce the mobility for future anastomosis, and care is taken to avoid dividing its lateral blood supply.

The cricothyroid muscle is elevated laterally to permit lateral division of the cricoid laminae. The proximal line of resection transects the cricothyroid membrane just inferior to thyroid cartilage and bevels laterally through the lateral laminae of the cricoid cartilage, usually more than halfway to a midlateral line. We then make a posterior cut at the inferior level of the cricoid cartilage, which may not resect the full extent of the posterior stenosis within the cricoid lamina. The stenosis within the cricoid then is resected off the posterior lamina once it is fully visualized with direct vision through the transected airway. A transverse cut against the posterior plate of the cricoid cartilage inferior to the vocal cords and arytenoid cartilages is made, leaving the denuded posterior plate of the cartilage intact. Removal of a portion of the posterior cartilaginous plate is sometimes necessary but risks injury to the recurrent laryngeal nerves. Preservation of at least the posterior perichondrium is required, and care must be used to avoid disrupting the cricothyroid joints superolaterally on the cricoid plate. It should be noted that depending on the patients age the cricoid may be significantly calcified and powered instrumentation may be necessary for precise resection.

The distal level of resection was determined earlier by endoscopic visualization. If the inferior border of the stenosis or tumor is in question, the initial transection always should be made slightly more superiorly because repeat resection more inferiorly is always possible. The first preserved ring is beveled backward from a high point in the anterior midline to the lower margin of that ring, creating an inverted U, and care is taken not to fracture this ring. At this point, a posterior membranous wall flap is formed to fit over the exposed posterior plate of the cricoid cartilage. The length of flap is determined by the amount of exposed posterior lamina. If needed, an additional anterior tracheal ring may be sacrificed to lengthen this posterior flap.

The shoulder roll then is removed and the field made orderly to prepare for closure. Endotracheal intubation is temporarily switched to cross-table ventilation to permit optimal access to the posterior wall closure. Four 3-0 Vicryl sutures are placed between the inferior margin of the posterior plate of cricoid cartilage to the base of the distal posterior tracheal flap. These sutures are clamped to the drapes such that they can be tied later in the order of the most anteromedial suture first, lateral suture second, and posteromedial suture last. Next, 4-0 Vicryl sutures approximate the tip of the posterior membranous wall flap of the trachea to the distal laryngeal mucosal line of resection within the cricoid cartilage. These sutures are placed from within the larynx, but the knots are arranged to lie outside the lumen and are clamped over the patient's head temporarily so as to avoid confusion with the external anastomotic sutures. Lastly, 3-0 Vicryl is used to complete the anastomotic closure, starting through the remnant of lateral cricoid cartilage to the second and third tracheal rings, followed by the thyroid cartilage to the first tracheal inverted U-ring. Tying of sutures begins after the patient is reintubated transorally and starts with the endolaryngeal 4-0 sutures, continues with the anteromedial sutures, and progresses laterally and posteriorly to the posterior midline. Strap muscles can be approximated over the anastomotic suture line, adding an additional layer of closure. Nonsuction drains are placed, the head is kept in a flexed position, and the patient is extubated immediately.

Tumor Resection

With tumors that occupy the laryngeal–tracheal junction, a resection similar to the type used to remove airway stenoses is employed. Benign tumors are removed with a minimal margin of normal tissue, whereas the rare malignancy confined to the endolaryngeal or endotracheal surface is removed with a margin dictated by the aggressiveness of the tumor. Preoperative imaging and initial endoscopy are used to determine the superior and inferior extents of the tumor, to rule out extralaryngeal and extratracheal extension, and to evaluate for distant metastasis.

The extent of the skin incision depends on the necessity of concurrent lymphadenectomy, which is performed before addressing the primary tumor. The larynx and trachea are exposed in an identical manner to the stenosis resection. Again, the superoanterior resection is made through the cricotracheal membrane to remove the anterior cricoid arch, curving laterally through the lateral cricoid laminae. An inferior incision then is made at the tracheal ring, which permits the tumor to be resected with a negative margin. At this point, a midline vertical incision is made to open the cricoid ring, and the upper tracheal rings are marked for resection. This allows optimal visualization before the posterior cuts are made. Although anterior tumors may be violated by this anterior midline incision, this does not preclude excellent tumor excision, albeit not adhering to the “no touch” tumor technique. In posteriorly placed tumors, the posterosuperior cut is made above the tumor site, with removal of underlying cricoid cartilage if the tumor requires. Again, the most common technique is drilling down the partial thickness of the posterior cricoid plate, although cricoarytenoid stability depends on preservation of the posterior perichondrium and a superior strut of cartilage on which the arytenoid articulates. The location of the inferior cut depends on two factors: it must be sufficiently inferior to allow for a negative tumor margin, and it should be made superiorly enough to form an inferiorly based posterior tracheal wall flap. If there is insufficient posterior tracheal wall to permit both these requirements, an additional anterior tracheal ring should be resected to generate more available posterior wall. A minimal posterior tracheal flap is needed for the repair of anterior tumor resections. The rest of the anastomosis and closure is identical to the stenosis repair detailed previously.

Superior Cricotracheal Tumor Resection

In patients with high subglottic tumor spread bordering on the undersurface of the true vocal fold or the interarytenoid area, the surgeon must be realistic in determining whether a laryngeal preservation operation is possible. Preoperative vocal fold fixation implies thyroarytenoid muscle involvement, cricoarytenoid joint fixation, or recurrent laryngeal nerve involvement, all contraindications to cricotracheal resection with laryngeal preservation. Nonetheless, cricoid tumors often will encroach either on the undersurface of the true vocal fold or the interarytenoid space, and surgical judgment must be used in determining the suitability of candidates for laryngeal preservation surgery. If the tumor is indeed judged to be favorable for resection, three modifications are made to the standard cricotracheal tumor resection technique. The first is a midline laryngofissure. This permits maximal tumor visualization, which is critical in such a location in which adequate margins are needed on the tumor, but postoperative laryngeal function depends on preservation of every millimeter of normal laryngeal structure. The second modification is the formation of a longer distal posterior tracheal wall flap to permit total resurfacing of the denuded posterior cricoid, even between the two arytenoid cartilages if required. This may necessitate resection of additional normal tracheal rings to generate sufficient length to reline the cricoid posterior wall. The last modification is placement of a temporary T-tube through the glottis for the initial 4- to 6-week postoperative period. The tube is placed with the proximal limb lying approximately 0.5 to 1.0 cm superior to the glottic level. The inferior limb can be quite short (2 cm). The horizontal limb is placed through a tracheotomy two rings inferior to the anastomotic line. Strap muscles are approximated to the area around the T-tube during closure to reinforce the airtight seal to prevent postoperative air leaks into the neck.

Nonsuction drains and a neck wrap are used to prevent postoperative fluid collections. In cases of cricotracheal resection without T-tube placement, patients are extubated immediately postoperatively. For patients with edema, one to two doses of steroid have been used to decrease swelling without significantly impairing anastomotic healing. Vocal cord function is assessed, and the neck is kept in a flexed position (pillows and strict nursing precautions usually suffice) for 2 weeks postoperatively. Patients are fed via nasogastric tube for 1 to 2 weeks, after which a swallow study is performed before starting an oral diet. Humidified air is used to decrease the risk of mucous plugs forming at the anastomotic suture line. If a laryngofissure and T-tube are used, the T-tube is removed under general anesthesia, during which time the airway is assessed endoscopically for patency and vocal cord motion, and any granulation tissue is removed. Although other authors are more aggressive with oral feeding, we do not start an oral diet until the T-tube has been removed.

Complications generally involve issues of either stenosis, failure of the anastomosis to heal, or vocal fold dysfunction. When stenosis at the anastomosis occurs, conservative treatment with dilation often can correct the obstruction. Repeat resection and anastomosis may be required if one suspects that a technical error occurred during the initial operation. Posterior glottic stenosis from scarring, from high resection, or from vocal fold immobility is a difficult problem to overcome. Often a laser cordotomy of the less mobile vocal fold will augment the airway sufficiently to permit unlabored breathing, albeit at the cost of good glottic competence, resulting in decreased voice quality. The most emergent and concerning complication is that of a nonhealing anastomosis. Patients with diabetes and those on steroids are the most susceptible to this complication, which, owing to the proximity of the great vessels, can be life threatening. Often the most prudent course of action is to retreat, placing a T-tube and giving antibiotics while the wound progresses, after which the airway is reassessed to determine if a tracheotomy-free airway is possible once the healing process is finished.

In 1998 Strome et al.¹⁶ led a team in performing the first successful total laryngeal transplantation. This operation was done for complete laryngeal stenosis resulting from trauma and included not only the larynx and pharynx but also the thyroid gland, parathyroid glands, and upper five rings of the trachea. Fourteen years after the transplant, due to a significant decrement in the patient's voice quality, we elected to explant the organ and rehabilitate the voice with a tracheoesophageal puncture.¹⁷ Further laryngeal transplants have been performed since 1998 adding to the body of evidence that this is a viable option for patients unable to undergo organ sparing surgery. Transplantation in the setting of cancer however, remains a barrier as a consequence of malignant potentiation from immunosuppression. Some suggest that the relative risk of developing a cancer while on immunosuppression can be as high as 400 fold that of the general population. The most common malignant lesions seen in transplant recipients are skin cancers, accounting for 37% of posttransplant tumors. The concern of posttransplant malignancy has prompted the development of newer agents with both immunosuppressive efficacy and tumor suppressive properties, such as the rapamycin derivative everolimus (40-O-[2-hydroxyethyl]-rapamycin) (RAD; Novartis Pharma AG, Basel, Switzerland). Everolimus is part of a family of immunosuppressants that targets the mammalian target of rapamycin (mTOR) kinase inhibitors. Its immunosuppressive and antitumor properties have been demonstrated in several animal and human cell lines, including squamous cell carcinoma. The efficacy of everolimus at preventing local and distant spread of cancer has been studied at our own institution, in a murine model, with good results as both a single, or combined agent.¹⁸ Until efforts at biomedical engineering are successful at developing suitable laryngeal replacements for laryngectomees dissatisfied with tracheal puncture, electrolarynges, or esophageal speech, reconstruction with autologous tissue in the setting of malignancy remains the greatest frontier for maximizing function after tumor ablation.

Cricotracheal resection for the treatment of airway stenosis is a highly effective and successful technique that can be used in the excision of neoplasms. Although squamous cell carcinoma is by far the most common malignancy of the upper aerodigestive tract, it is rarely suitable for resection with the cricotracheal resection method. Squamous cell carcinoma, in particular, should be treated early and aggressively due to a propensity for nodal and distant metastasis, and poorer outcomes with advanced disease. Other malignancies and several benign tumors of the subglottis and upper trachea are especially amenable to cricotracheal resection, and excellent voice, airway, and swallowing results can be achieved. Cricotracheal resection and reconstruction often requires collaboration between otolaryngology and thoracic surgery services, with the main goals being a good oncologic result, while preserving as much normal laryngotracheal anatomy and physiology as possible; including the recurrent laryngeal nerves. Allogenic transplantation is on the horizon of new technologies allowing complete upper aerodigestive tract reconstruction in the face of radical tumor ablation.

B.J. is a 62-year-old woman who presented with a 1-year history of progressive dyspnea. A CT scan revealed a right-sided thyroid goiter, and she was referred for removal of the mass. On office examination, the patient was not notably hoarse but did demonstrate moderate biphasic stridor. Further review of the CT scan demonstrated a fullness to the right subglottis without destruction of the underlying cricoid cartilage (Fig. 63-4A). Flexible fiberoptic nasal laryngoscopy demonstrated both deviation of the laryngotracheal complex to the left and a narrowed subglottic airway with a lesion on the posterior right subglottis (Fig. 63-4B). Operative management began with direct laryngoscopy and biopsy of the subglottic mass, revealing adenoid cystic carcinoma. A transcervical right thyroid goiter biopsy then was performed, demonstrating a benign thyroid goiter on frozen section.

Since the lesion was present high on the undersurface of the right true vocal fold and posterior cricoid lamina, a cricotracheal resection was accomplished with an accompanying laryngofissure. Partial thickness of the inferior cricoid cartilage was drilled down for an additional deep margin. Division of the thyroid cartilage was performed not only for optimal visualization of the tumor to obtain negative margins but also to allow reconstruction with a posteriorly based tracheal flap and placement of a temporary T-tube (Fig. 63-3). One tracheal ring was resected to obtain total tumor removal and to form a posterior tracheal flap. Level VI (mediastinal) lymph nodes were resected and demonstrated no regional metastases. The patient was allowed to take an oral diet 2 weeks postoperatively without significant dysphagia despite the end of the superior limb of the T-tube lying above the glottic aperture. She received 7200 cGy of radiation to the area starting 4 weeks postoperatively. The T-tube was removed at the end of radiation, and the patient demonstrated a good voice and excellent airway. She was followed postoperatively with routine imaging and fiberoptic examinations to check for local recurrence. Approximately 3 years after surgery she was found to have an asymptomatic lung metastasis on PET scan, and the patient succumbed to her distant disease 7 years after her surgery, with no local recurrence.

Any resection of the proximal trachea and cricoid likely results in swelling and merits consideration of placing a small uncuffed tracheostomy distal to the anastomosis unless a T-tube is placed. We generally have a thoracic surgeon and otolaryngologist collaborate on these procedures at the Brigham and Women's Hospital to optimize results. A bronchoscopy on postoperative day 7 is useful to clear secretions and evaluate the anastomosis. On occasion we identify early sloughing of mucosa which can be debrided.

The suturing of a posterior mucosal flap on the denuded back wall is challenging technically. The goal is to get the mucosa to attach there, and a few carefully placed sutures suffice.