Natural Orifice Total Transtracheal Endoscopic Thyroidectomy Surgery: First Reported Experiment

Abstract

Background:

Natural orifice translumenal endoscopic surgery (NOTES^®; American Society for Gastrointestinal Endoscopy [Oak Brook, IL] and Society of American Gastrointestinal and Endoscopic Surgeons [Los Angeles, CA]) is an improvement in surgical interventions. In this study we developed an innovative transtracheal endoscopic thyroidectomy technique and explored its feasibility in animal models.

Materials and Methods:

Transtracheal endoscopic thyroidectomy was performed in anesthetized dogs and pigs. The endoscope was advanced into the pretracheal space via a longitudinal incision on the anterior tracheal wall. Hemithyroidectomies and partial lobectomy were performed using special double-lumen endotracheal tubes and conventional endoscopic instruments. The tracheal wall incision was closed using absorbable sutures, and the animals were sacrificed at Day 5 postsurgery.

Results:

Hemithyroidectomy and partial thyroidectomy were successfully performed on pigs and dogs. The average operative time for each model was 69.4 minutes. No significant complications were encountered during surgery.

Conclusions:

The transtracheal endoscopic thyroidectomy technique is feasible and has the potential to be an alternative method for other types of thyroid surgeries.

Introduction

The first attempt of natural orifice translumenal endoscopic surgery (NOTES^®; American Society for Gastrointestinal Endoscopy [Oak Brook, IL] and Society of American Gastrointestinal and Endoscopic Surgeons [Los Angeles, CA]) was reported in 2004 by Kalloo et al.¹ NOTES is an less invasive procedure that uses natural anatomical passages to gain access to the intraabdominal organs and has potential advantages, including smaller skin incisions, reduced postoperative pain, and earlier postsurgery recovery. The total transtracheal endoscopic thyroidectomy (TTET) is inspired by NOTES and is the latest innovation in neck surgery. Previous approaches in thyroid surgery have their own drawbacks in terms of cosmetic viewpoint (e.g., cervical scars), invasiveness, and scar-related complications.^2,3 Therefore, TTET is considered as a surgical modality that is beneficial to patients with thyroid disease who wish to have neck surgery without leaving a scar.

We have carried out NOTES experimental research in animal models since 2007 and have successfully applied transvaginal endoscopic cholecystectomies in patients. Inspired by the advantage of transvaginal NOTES cholecystectomies,⁴ our group focuses on the application of NOTES in neck surgery. We have created an innovative transtracheal NOTES procedure to access the thyroid region, which is the closest feasible entry into the thyroid gland. This is the first study to perform TTET without an accessory skin incision in pig and dog animal models.

Materials and Methods

The experimental procedures were performed on three domestic female pigs (median age, 4.8 months; range, 4–6 months) weighing 40–45 kg and fourteen Beagle dogs (8 males, 6 females; median age, 1.8 years; range, 1.6–2.1 years) weighing 15–20 kg. The experimental procedures were approved by the Animal Ethical Committee of Shandong University, and the experiments were conducted in accordance with the Natural Orifice Surgery Consortium for Assessment and Research regarding animals.⁵

Endoscopic and laparoscopic tools

Endoscopic tools included a flexible fiber optic bronchoscope (external diameter, 4.2 mm) (Pantax Surgical, Tokyo, Japan) and an endoscopic biopsy forceps (Olympus Surgical, Tokyo). Laparoscopic tools included endoscopic hook cautery and a bent laparoscopic instrument (Roticulator™ Endo Mini-Shears™, Roticulator Endo Dissect™, and Endo Stitch™ suturing device; all from Covidien, Mansfield, MA).

Animal preparation

The animals (pigs and dogs) underwent general anesthesia (10 mg/kg pentobarbital, intravenous administration). Endotracheal intubation was performed transorally using the Laser-Flex^® tube with dual cuff (Covidien). The endotracheal tube was inserted into the level of the 10th–12th tracheal rings to prevent liquid obstruction during the thyroid resection.

Operation procedure

Anesthetized animals were placed in the supine position with the neck slightly extended to avoid tracheal flexion throughout the procedures. All animals inhaled saline aerosol that contained dexamethasone and gentamicin once per hour before and during the procedures.

The ventral midline skin of the neck from the larynx to the manubrium was suspended by adhesive plaster to create sufficient operating space (Fig. 1). The instrument and endoscopic flexible fiber optic bronchoscope were inserted into the operating field above the ventrolateral main stem of the Laser-Flex tube (Fig. 2). All procedures were performed under endoscopic vision.

FIG. 1.

The pig was placed in the supine position with neck extension, and its neck was lifted up by adhesive plaster.

FIG. 2.

A labeled diagram showing the positioning of the instruments, the tracheotomy site, and the thyroid gland.

The airway surface extending from the caudal cricoid cartilage to the seventh tracheal ring was sterilized using povidone–iodine (2.5 mg/mL) cotton swabs. The thyroid gland was detected by endoluminal ultrasonography in the trachea and marked with hook cautery at the same time. The anterior wall was longitudinally incised for the length of four rings along the midline using hook cautery (Fig. 3) and laparoscopic scissors. A minimal length of dissection of four rings was made to facilitate the entrance to the pretracheal space. Meanwhile, the plane of the thyroid fascia was directly accessed from the dorsal aspect, and the operating space was established by free inflatable suspension using adhesive plaster.

FIG. 3.

Endoscopic view of a longitudinal incision on the anterior tracheal wall made with the hook as the transtracheal access to the pretracheal space.

The transtracheal access to the pretracheal space in animals was established, and the thyroid gland was exposed between the strap muscles of the sternocephalicus and sternohyoideus ventrally and the muscle of the sternohyoideus laterally. The division of the thyroid parenchyma and cauterization of the vessels were achieved using the Roticulator endodissector and shears. During this procedure, we carefully carried out dissections to identify the inferior thyroid artery and recurrent laryngeal nerve in the tracheoesophageal groove and maintained a distance of at least 2 mm from the major neurovascular structures. The superior thyroid artery was incised close to the upper lobe of the thyroid gland to avoid damage to the internal branch of the upper laryngeal nerve. The inferior thyroid artery was divided and incised near the thyroid gland to avoid the injury to the recurrent laryngeal nerve. The thyroid gland was separated from the external parathyroid gland and the cranial thyroid artery branches that supply the parathyroid gland. The thyroid gland and its capsule were removed, while the external parathyroid gland was kept intact.

For the cases in which partial thyroidectomy was intended, division of the thyroid parenchyma was achieved exclusively with the endodissector without dissection of the feeding vessels. During the procedure, the endoscopic forceps (Fig. 4) was used to advance along the side of the endoscope to obtain tissue or debris. Following thyroidectomy, the resected specimen was extracted through the tracheal incision (Fig. 5), and the longitudinal opening of the anterior tracheal wall was closed from the distal to proximal direction using the Endo Stitch suturing device (Fig. 6). After the first surgical knot was ligated outside the tracheal lumen, the needle of the Endo Stitch was passed through the external layer of the anterior wall of the exposed trachea. The last surgical knot (the most proximal one) was ligated in the intratracheal area, and the needle was passed under the ligature of the second most proximal knot. Therefore, each knot (with the exception of the most proximal one) remained outside the lumen, and the anterior wall of the trachea sealed the suture.

FIG. 4.

The thyroid gland was dissected under endoscopic vision.

FIG. 5.

The resected specimen was extracted by endoscopic forceps.

FIG. 6.

Closure of the tracheal incision by absorbable running sutures.

At the end of the procedure, the tracheal incision was washed with saline, and the drainage was removed. The final visual inspection revealed no abnormalities.

Results

In all described cases, TTETs were successfully completed. The cases included 26 thyroid lobectomies and 8 partial thyroid lobe resections. The mean operative time was 69.4±21.7 minutes (range, 55–137 minutes). The mean operative blood loss was 12±3.8 mL (range, 5–35 mL).

There was no perioperative morbidity. All the animals were immediately extubated at the end of the operation. The last evaluated endoscopic follow-up was performed at 5 days postoperatively (Fig. 7), and it showed a perfect healing process of the operation without signs and symptoms of tracheal stenosis. All animals were sacrificed, and the postmortem histopathology examinations showed normal healing after surgery.

FIG. 7.

Endoscopy image of tracheal incision at 5 days after operation.

Discussion

The rapid development of thyroid surgical techniques is largely due to the increased incidence of thyroid diseases in young to middle-aged women, who usually pay great attention to the cosmetic results after thyroid surgery. The most important goal in thyroid surgery is to avoid the visible scar in any natural position. To simplify the description of the different techniques of thyroidectomy, we divided them into two categories: with-scar surgery and without-scar surgery (NOTES). With-scar surgery includes minimally invasive video-assisted thyroidectomy (MIVAT)^3,6 or endoscopic techniques used for the treatment of thyroid disease in the past 10 years.

MIVAT was first described by Yeung⁶ in 1998, and the technique was perfected by Miccoli et al.³ for the transcollar approach with the use of endoscopic techniques and was performed with an incision length of 15–20 mm.⁷ However, only a subset of patients is appropriate for the MIVAT approach. Conventional thyroidectomies are still performed in most patients with large goiters and advanced cancers.⁸ The main limiting factor of the MIVAT approach is the length of the procedure and the skin incision lengths, depending on the volume of the specimen and the gland obtained at the surgical resection.^9,10 It is a larger-scale operation,¹¹ and its potential drawback is a determinant for cosmetic result. The common postoperative symptoms include dysphagia or a pulling sensation during neck extension.

Endoscopic thyroidectomy, which is part of the scar surgery, was first performed by Hüscher et al.¹² Endoscopic surgeries can be divided into various approaches, according to the position of the incision,¹³ such as the lateral neck,^14,15 anterior chest,¹⁶ breast,^17,18 axillary,^20,21 and various combinations of these approaches.^22,23 There is no doubt that the aim of these methods mentioned above is to achieve an ideal cosmetic result.^19,²² However, these techniques may cause subcutaneous hematomas, emphysema, or widespread skin scars. Endoscopic thyroidectomy with different approaches may be considered as “minimal access” but not “minimally invasive.” Meanwhile, the variety of endoscopic approaches applied in thyroidectomy may imply that the optimal technique and the best instruments have not yet emerged.

The philosophy of thyroid surgery dramatically changed when Kalloo et al.¹ demonstrated the first successful NOTES technique. NOTES, also called no-scar surgery, represents a quantum leap in the endeavor to achieve cosmetic intactness.²⁴ In neck surgery, Witzel et al.²⁵ were the first to demonstrate the feasibility and safety of transoral access in the endoscopic thyroidectomy approach in both human cadavers and animal models. However, this technique is not a real natural orifice surgery, but a hybrid technique due to the additional skin incision below the larynx to allow the insertion of a fixation forceps through a 15-mm trocar. Since then, exciting creativity and research have followed at a stunning rate. The first report of an entirely natural orifice surgery—the totally transoral video-assisted thyroidectomy technique—without any accessorial incision of the skin applied in hemithyroidectomy has been proposed by Benhidjeb et al.²⁶ However, this technique has some complications, including gas insufflations, obstacle to oral intake, risks of infection, and laryngeal nerve injury.²⁷

Recently, we performed a TTET as a natural orifice surgery technique that has never been previously reported in the literature. In this approach, an entirely endoscopic technique allows direct access to anatomically defined surgical pretracheal spaces in the anterior neck region without any visible skin incisions. A distinct advantage is the absence of a wound on the anterior neck compared with the endoscopic thyroidectomy and MIVAT method practiced by Miccoli et al.,³ which could potentially lead to scar-related issues. This procedure could also prevent or minimize postoperative sequelae, like swallowing disorders, in terms of maintaining the right layer behind the hyoid bone and the strap muscles. Furthermore, we were able to perform thyroidectomies by applying adhesive plaster to suspend the midline skin of the anterior neck instead of insufflations of carbon dioxide (CO₂) gas. The operating space created was big enough to operate safely under endoscopic vision in the animal trial. Meanwhile, such a gasless approach prevents the CO₂-related complications.¹⁵ We used the adhesive plaster method to lift the skin in front of the trachea, which will not cause any obstacle in tracheal surgery; however, this approach cannot be used in abdominal surgery due to the large space requirements in abdominal surgery.

Another vital issue in thyroid surgery is safeguarding of the recurrent laryngeal nerve.^10,28 We distinguished this nerve intraoperatively only under endoscopic vision rather than using the neuromonitoring system.^8,28,29 It can reduce the expenses and simplify the operation. Our experience with traditional thyroidectomy in humans and the transtracheal access in this study shows that the recurrent laryngeal nerve is easier to identify in the endoscopic procedure²⁵ than in open surgery because of the views transmitted by optical magnification.

The method of reliable tracheotomy closure might be critical in the TTET technique like in other NOTES procedures, but we have successfully used transtracheal NOTES Endo Stitch and achieved more efficient closure. This technique eliminated the need for complex tissue manipulation and expensive airway silicone stent placement.^30,31 It also provides watertight closure with a minimal complication rate. This technique might simplify the process of tracheotomy closure and achieves a result as reliable as a full-thickness tissue approximation. The follow-up endoscopies showed good healing of the tracheal openings.

Other major concerns in thyroid surgery are to decrease potential tracheotomy complications and to make the procedure safer. We did not observe any major or minor complications in this study. All animals showed normal postoperative behaviors 5 days postoperatively, in terms of pain, food intake, and social behavior,^7,32 which prove the feasibility and safety of this new procedure. In general, we monitor the animals for 1–3 months posttracheotomy; however, in our experiment the tracheal incisional closure was a continuous longitudinal suture, and hence it will not cause any obstacle to the blood circulation or cause ischemia. Therefore, we did not perform longer-term posttracheotomy observation.

Complications in the tracheostomy procedures range from intraoperative to late postoperative state. The major intraoperative and early postoperative complications include infection, bleeding, subcutaneous emphysema, laryngeal edema, stenosis, tracheomalacia, ulceration granuloma, and blocking of the tube. To prevent or minimize these complications, we have used a new endotracheal tube. This special endotracheal tube has an inflated low-pressure cuff, and the upper cuff is packed with gauze sponges. This tube not only provides a delivery system for oxygen and instruments, but also prevents blood, irrigation fluid, exudates, and tissue from winding up in the lungs during the procedure. The size of the orotracheal channel tube is large enough to allow adequate gas delivery around the endoscope, and the channel tube for other instruments allows all standard laparoscopic instruments to pass through it.

However, the absence of postoperative complications, such as paresthesia or hematoma, cannot be classified as an outcome of this study due to the restriction of our study. For example, if there is any tracheal calcification after incision, it may cause tracheal stenosis. Therefore, we did not perform this surgical technique in animals with tracheal calcification. In our future study, we will explore whether abscess formation will be a problem with transtracheal thyroid surgery.

NOTES is still in developmental stages. Further investigations are required to evaluate the pros and cons of this procedure. For instance, a careful evaluation of the risk of infection needs to be done because neck surgery can possibly turn from an aseptic operation to a potentially infectious surgical intervention by the spread of pathogenic germs of the transtracheal microflora.²⁶ Therefore, animal experiments are required to evaluate the prevalence of infection and bacterial contamination. If there is no increase in infection in animals, the transtracheal thyroid surgery then can be evaluated in a prospectively controlled clinical setting.

In conclusion, endoscopic thyroidectomy via a total transtracheal route is an easy approach and represents a notable improvement in the surgical techniques of neck surgery. However, due to the differences between the animal and human anatomies, we suggest conducting further studies using fresh human cadavers before the thyroidectomy is actually applied in human patients. In consideration of the individual anatomical differences that exist in each human body or cadaver, the location of the thyroid gland related to the trachea is different. The location of the thyroid isthmus can be determined using ultrasound, and then the incision can be made below the tracheal rings to allow a smooth entrance to the pretracheal space. It will not only avoid damage to the inferior thyroid artery, azygos vein, and plexus venosus, but also indicate the accurate location of the tracheal rings beneath the thyroid gland to reduce unnecessary tracheal damages.

We believe that this new method is worthy of further investigation, as it is technically feasible and can be easily applied in the management of thyroid diseases. To the best of our knowledge this is the first report on transtracheal endoscopic thyroidectomy as a natural orifice surgery application in thyroid surgery.

Footnotes

Acknowledgments

This work was supported by The National Postdoctoral Foundation of China (grant 20090451318), the Youth Foundation of Shandong Province (grant 26010105201118), and the Jiangxi Province Science, and Technology Support Program (grant 20122BBG70119).

Disclosure Statement

No competing financial interests exist.

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