Surgery for Thyroid Cancer Invading the Trachea

Abstract

Thyroid cancer invading the trachea can be asymptomatic, but when tumour invasion reaches the mucosal surface, it causes bloody sputum and dyspnoea. The treatment plan for thyroid cancer is determined based on the site, depth, and extent of the invasion. Different from tumours arising from the tracheal mucosa, in thyroid cancer, invasion begins outside the airway and progresses toward the lumen, making it difficult to accurately diagnose the extent of the invasion even with bronchoscopy. Therefore, surgeons must determine the range of resection during surgery. Invasion reaching the tracheal mucosa requires full-thickness resection and is performed using tracheal window resection combined with tracheocutaneous fistula or tracheal sleeve resection followed by end-to-end anastomosis. The airway is safely secured with window resection, but closing the tracheal stoma often requires multi-stage reconstruction. Sleeve resection is an oncologically appropriate surgical method that can be completed in one stage, although there is a risk of serious complications associated with anastomotic dehiscence. Since well-differentiated thyroid cancer progresses slowly, some degree of survival can be expected even with incomplete resection. However, when shaving is performed for tumours with deep invasion that reaches the tracheal mucosa, the residual tumour tissue continues to grow steadily and eventually leads to airway stenosis. Since reoperation for tracheal resection is difficult, radical full-thickness resection should be performed in the initial surgery. Although this surgical intervention is far more demanding for both patients and surgeons than shaving, the procedure eventually improves patient’s prognosis and quality of life.

Introduction

The frequency of thyroid cancer invading the trachea is 1–8% and is found in 10–20% of cases of local recurrence [1, 2]. Thyroid cancer is often asymptomatic even when the tumour is invading the trachea, but once the tumour invasion reaches the mucosal surface, it causes bloody sputum and dyspnoea. Therefore, even when distant metastasis is present, it is often best to resect the lesion invading the trachea to achieve local control. Since well-differentiated thyroid cancer usually has an indolent course, the prognosis is expected to be good with full resection; furthermore, some degree of survival can be expected even with incomplete resection. In addition, full-thickness tracheal resection requires reconstruction and possibly results in serious complications associated with anastomotic dehiscence or vocalization, both of which are directly related to the patient’s quality of life (QOL). These two factors make it difficult to determine the surgical indications.

Our department has been performing proactive respiratory interventions for airway stenosis due to recurrent thyroid cancer, including endoscopic tumour ablation [3] and tracheal stent placement [4], with almost all patients undergoing incomplete resection in the first operation to ensure a good QOL postoperatively. Due to our extensive experience with such cases, we believe that complete resection in the first operation is the key to improve the patient’s prognosis and QOL, and we select surgical methods aimed at local curability.

In this paper, we described the latest findings on controversial surgical treatments for tracheal invasion of well-differentiated thyroid cancer.

Patterns of Tracheal Invasion

The presence or absence of tracheal invasion and its severity are factors that affect prognosis [5, 6], and understanding the pattern of tracheal invasion by the tumour is important for developing a treatment strategy [7]. Shin et al. have performed full-thickness tracheal resection on 22 patients with papillary carcinoma invading the trachea and described the patterns of progression of tracheal invasion [5]. Tumour invasion begins in the annular ligaments between the tracheal cartilage and progresses vertically. Once the tumour reaches the submucosal tissue, it progresses circumferentially and craniocaudally, eventually invading beyond the mucosa (Fig. 1). The degree of tracheal invasion is classified into four stages based on the depth from the wall (stage I: up to the perichondrium, stage II: annular ligament or tracheal cartilage, stage III: lamina propria, and stage IV: mucosal epithelium).

Fig. 1.

Tracheal invasion patterns and staging. Shin et al. have classified tracheal invasion into four stages according to the depth of tracheal wall invasion [5]. Stage I, tracheal adventitia or perichondrium; stage II, cricoid ligament or tracheal cartilage layer; stage III, lamina propria (reaching the mucosa); and stage IV, mucosal epithelium (mucosal invasion). L, annular ligament

Different from tracheal cancer, which arises in the tracheal mucosa and spreads to the surrounding area, in thyroid cancer, invasion begins outside the wall and progresses toward the mucosal surface of the lumen. Because bronchoscopy provides observations from the lumen, which is the most advanced part of the invasion, when there is mucosal invasion, the extent of it is often greater in the tracheal adventitia than in the tracheal mucosa (stage IV) [8].

Surgical Strategies for Tracheal Invasion (Shallow Invasion): Shaving

In developing a surgical strategy for tracheal invasion, it is important to perform three-dimensional assessments of the invasion with computed tomography and endoscopy. This is to diagnose (1) the location of invasion, (2) the depth of the invasion, and (3) the extent of the invasion longitudinally and circumferentially. Shaving is a method of scraping the tracheal wall at the invasion site tangential to the trachea without opening the tracheal lumen. When invasion has reached the adventitia or perichondrium but not the cartilage layer (Shin’s stage I), there is a consensus that it is sufficient to shave the periphery of the cartilage layer while ensuring support for the airway is maintained [9]. Next, the invasion reaches the annular ligament or cartilage layer but not the tracheal mucosa (stage II). When shaving at this depth, an accurate diagnosis of the extent of invasion is clear only after surgery; thus, some authors have recommended full-thickness resection to ensure negative histological margins [10, 11]. Therefore, because full-thickness resection requires reconstruction after resection, other surgeons perform shaving, which is a substantially less invasive technique with far fewer complications. Although shaving may lead to tumour tissue remaining on the resection margin, the rate of local recurrence after shaving is approximately 5% over 7 years (mean) [12–14].

However, there has been no prospective study comparing surgical methods for tracheal invasion [15]. Previous reports have retrospectively compared incomplete resection (shaving) of the trachea with complete resection. That is because surgeons operate as needed according to the extent of tracheal invasion found during surgery; therefore, the differences in surgical approaches may simply reflect differences in surgical stage or pathological condition. There have been no studies comparing the superiority or inferiority of surgical methods in cases at the same stage of progression. In particular, an international consensus has yet to be reached on how to treat shallow tracheal invasion in which the wall depth does not go beyond the cartilage layer.

Surgical Strategies for Tracheal Invasion (Deep Infiltration): Window and Sleeve Resection

When tumour invasion reaches the mucosa beyond the cartilage layer (deep infiltration) (i.e., into the lamina propria [stage III] or mucosal epithelium [stage IV]), full-thickness resection of the airway structure is required [16].

The types of full-thickness resection include window resection and sleeve resection (Fig. 2). Window resection is the partial resection of the trachea with a safety margin in the area of tracheal invasion (Fig. 2a). The tracheal defect is sutured to the skin of the neck to create a tracheocutaneous fistula, and the fistula is closed as usual in two stages. If the resection range is a small defect that is no more than one-third the circumference of the trachea, it can be reconstructed with a local flap (Fig. 3a). When the defect exceeds one-third of the circumference of the trachea and four cartilage rings in the longitudinal direction (2 cm), hard reconstruction is necessary to avoid a collapse of the soft-tissue roof and to preserve the lumen [1, 16]. Autologous tissues used for reconstruction include auricular cartilage grafts [18], composite nasal septal grafts [19], rib cartilage grafts [20], and pedicled sternocleidomastoid clavicular periosteocutaneous flap [21, 22] (Fig. 3b). Furthermore, when the extent of tracheal defect is even greater and exceeds half the circumference, both reconstructions of the anterior and lateral walls is necessary (Fig. 3c). In such cases, creating a framework that both sustains the lumen and possesses elasticity is challenging, and it may be impossible to close the tracheal stoma [23]. Hard reconstruction is a multi-stage operation in which the lumen and framework are gradually built up and the process is finally completed by closing the lumen. Because multiple operations are necessary, the disadvantage is the considerable amount of time it takes to complete the procedure, but the advantage is that adjustments can be made safely and reliably while observing the tracheal lumen.

Fig. 2.

Window resection and sleeve resection. a Window resection, b sleeve resection, c step-like sleeve resection. 1st, the first tracheal ring

Fig. 3.

Tracheal defect ranges and reconstruction methods, modified from a previous study [17]. a Tracheal defect is up to one-third tracheal circumference, b tracheal defect is one-third to one-half circumference, c tracheal defect exceeds one-half circumference

Sleeve resection is a full-circumference resection of the trachea, including the tumour, involving an incision of the annular ligaments between the tracheal rings (Fig. 2b). Reconstruction is performed by end-to-end anastomosis. Ozaki et al. have histologically examined the spread of tumours in the tracheal walls of 21 patients who underwent tracheal resection for thyroid cancer, revealing that in the longitudinal direction, invasion on the mucosal side of the trachea did not exceed the adventitia, but in the circumferential direction, invasion on the mucosal side beyond the adventitia was common [24]. Furthermore, sleeve resection is recommended because window resection following the extent of thyroid cancer invasion on the adventitia side of the trachea is associated with tumour tissue remaining on the resection margin. In contrast, in many cases, sufficient local control can be obtained only through window resection, and there are no data indicating window resection has a higher local recurrence rate than sleeve resection [1, 2].

Obtaining a negative surgical margin is easy with sleeve resection combined with end-to-end anastomosis; the procedure is completed in one stage and has superior cosmetic results. Functionally, after reconstruction, the tracheal lumen is covered with normal tracheal mucosa. This process is different from window resection, which involves the placement of a skin flap to close the tracheal defect while also preventing any difficulty in the expectoration of airway secretions. Although sleeve resection is, thus, theoretically superior, the postoperative complications are not negligible, ranging from 15 to 39%, and its postoperative mortality rate is 1.2% [25]. The most serious complication of this procedure is anastomotic dehiscence. The incidence rate of anastomotic dehiscence with tracheal sleeve resection is 0–11%, followed by arterial rupture and mediastinitis, which have been reported to lead to surgery-related deaths in some cases [24, 26–28]. The two main causes of anastomotic dehiscence are local infection and excess tension on the anastomotic site. The first cause, local infection, occurs from the tracheostomy. Often in thyroid cancer invading the trachea, the invading tumour has already caused unilateral vocal cord paralysis, and the risk of bilateral paralysis increases from the extensive operative exposure of the bilateral recurrent laryngeal nerve used with this method. This is a significantly different point from sleeve resection for primary tracheal tumours. The tracheostomy is made as caudal as possible to reduce the impact on the anastomosis, but they are often still not sufficiently far apart. To prevent sputum contamination around the tracheostomy opening, the strap muscles are sutured around the opening to create a tracheocutaneous fistula. Even with these additional procedures, the risk of decrease in blood supply and infection of the anastomosis cannot be avoided, which may lead to anastomotic dehiscence. We adopt intraoperative nerve monitoring and avoid sleeve resection when bilateral vocal cord paralysis, including transient cases, is anticipated. The second cause of anastomotic dehiscence is excess tension on the anastomotic site. During surgery, the trachea is mobilized to reduce tension on the anastomosis (tracheal release). When the blunt dissection of avascular pretracheal plain is performed to the level of the carina, three cartilage rings of the mediastinal trachea can be mobilized at the neck [29]. Furthermore, when the neck is placed in maximum anteflexion, it brings six cartilage rings of the trachea close together. Therefore, if the tracheal resection is not over 4 cm (eight cartilage rings), usually, suprahyoid laryngeal release associated with temporary dysphagia and aspiration is not required [30]. Some surgeons use two stiches placed in the submental crease and through the upper thoracic skin during the postoperative period to maintain anteflexion postoperatively, whereas others perform tracheal intubation and systemic management with a ventilator under sedation for approximately a week to maintain even more stable anteflexion and secure the airway. This makes postoperative respiratory complications, such as pneumonia and atelectasis, more likely to occur.

As such, tracheal resection with end-to-end anastomosis is not necessarily the best surgical approach due to the complexity of postoperative airway management and the possibility of fatal problems caused by anastomotic complications. In contrast, tracheal window resection requires a multi-stage surgery to complete the airway, and because the surface of the reconstructed tracheal lumen is not the tracheal mucosa, there are various disadvantages, such as sputum accumulation, scab formation, adhesion, and granulation formation at the mucocutaneous suture site. In contrast, because a tracheal stoma is created, the airway is reliably secured and significantly safer than with sleeve resection [31]. In addition, airway management is simple because there is no need for anteflexion fixation.

For these reasons, realistically, there is a little need to consider the oncological assessment when deciding between sleeve resection and window resection, and instead, the approach is usually determined by taking into account not only the site and extent of the invasion but also the patient’s ability to tolerate surgery, expected prognosis, and skills and experiences of the medical team involved. Table 1 shows the indications and limitations of the surgical approaches for thyroid cancer invading the trachea. Indications for sleeve resection, which involves a high level of perioperative risk, should be determined carefully for each patient. Window resection is safer for patients with a history of external irradiation of the neck or complicated with poorly controlled diabetes mellitus in particular. In addition, older patients often have lower reserves, which increases the risk of complications associated with sleeve resection.

Table 1.

Indications and limitations of surgical approaches for thyroid cancer invading the trachea

Approach	Indications		Limitations	Features
	Tracheal wall depth	Invasion range
Shaving	Superficial invasion: to the tracheal adventitia and perichondrium (Shin’s stage I)	Small range	Invasion to the annular ligament or tracheal cartilage (stage II)	Less invasive
Window resection combined with construction of tracheocutaneous fistula	Deep invasion: into the tracheal mucosa (stages III and IV)	Invasion of the anterior tracheal wall	Circumferential direction: up to half the circumference, longitudinal direction: up to four rings (2 cm), difficult with invasion to membranous portion	Multi-stage reconstruction
Sleeve resection combined with end-to-end anastomosis	Deep invasion: into the tracheal mucosa (stages III and IV)	Circumferential direction: invasion exceeding half the circumference	Partial resection of the cricoid cartilage (one-third the circumference) on the cranial side and up to eight rings (4.5 cm) longitudinally is safe	Risk of serious complications (anastomotic dehiscence)

Tracheal Step-Like Sleeve Resection

During performance of tracheal sleeve resection, when the tumour invasion does not extend to the first tracheal ring, the annular ligaments are resected on the cranial and caudal sides of the tracheal cartilage invasion to perform end-to-end anastomosis. The problem here is that with thyroid cancer, tumour invasion commonly occurs in the first tracheal cartilage ring [4]. Because the recurrent laryngeal nerve enters the larynx at the inferior margin of the cricoid cartilage, if a horizontal resection line is set between the cricoid cartilage and the first tracheal ring, the anastomosis will be placed at the recurrent laryngeal nerve entry site, which increases the risk of recurrent laryngeal nerve paralysis on the healthy side. In such cases, a safe option is the ‘step-like sleeve resection’, which has a resection line that preserves the first tracheal ring on the healthy side (Fig. 2c). As a result, the trachea on the affected side is anastomosed to the cricoid cartilage. Figure 4 presents a case of step-like sleeve resection for tracheal invasion of papillary thyroid cancer.

Fig. 4.

Tracheal step-like sleeve resection. A woman in her 50 s visited our hospital complaining of hoarseness and was diagnosed with papillary carcinoma of the right thyroid lobe by aspiration cytology. The tumour had invaded the tracheal mucosa and extended mainly from the right wall to the posterior wall. Thus, window resection would have been difficult, and tracheal sleeve resection was indicated. Total thyroidectomy and right modified neck dissection were performed, followed by step-like sleeve resection of tracheal cartilage rings 1–4 combined with end-to-end anastomosis. a Computed tomography findings: a 3-cm-diameter tumour invading the trachea is observed on the right thyroid lobe (black arrow). b Preoperative bronchoscopy findings: tumour invasion is observed from the right side of the trachea to the membranous portion. c Intraoperative findings: as tumour invasion on the right extended to the first tracheal ring, step-like sleeve resection was performed. d Postoperative bronchoscopy findings: 1 month later, sutures are observed from the right side of the trachea to the membranous portion in front, and on the left, the suture line is visible in the back

Conclusion

Although there has been a significant debate over the surgical approaches for thyroid cancer invading the trachea, based on recent advancements in three-dimensional assessments, more conservative approaches that are suited to the gradual progression of tumour invasion are now commonly selected. Meanwhile, surgeries that clearly leave behind local tumour tissue should be avoided, and if the best approach is beyond the skill of the medical team in charge, referral to a more experienced institution should be considered.

For tracheal invasion of thyroid cancer, the choice between shaving and full-thickness resection is determined based on the depth of the invasion, and in full-thickness resection, the extent of the resection is determined by the longitudinal and circumferential extent of the invasion.

Sleeve resection, which is an oncologically appropriate surgical method, may be the ideal choice. Realistically, however, more important than choosing between sleeve resection and window resection for patients who need full-thickness resection is to not settle for surgeries that insufficiently resect the tumour, such as shaving, in the name of preserving the patient’s postoperative QOL. Fully resecting the tumour in the first operation is the most important step to improve the patient’s prognosis and QOL.

Data and Materials Availability

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Declarations

Conflict of Interest

The authors declare no competing interests.