Clinical Applied Anatomy in Trans-Areolar Endoscopic Thyroidectomy: Crucial Anatomical Landmarks

Abstract

Introduction:

Endoscopic thyroidectomy (ET) has been successfully established as an excellent surgical approach. This study summarizes and describes the crucial anatomical landmarks for clinical applied anatomy in trans-areolar ET, which may help further improve the quality and safety of trans-areolar ET.

Materials and Methods:

Five hundred forty patients who underwent trans-areolar ET from January 2015 to June 2018 at our institution were evaluated. Several crucial anatomical landmarks were described during the surgical procedures. The surgical outcomes, including the operative time, conversion, intraoperative blood loss, postoperative complications, and postoperative stay, were collected.

Results:

All patients successfully underwent trans-areolar ET without conversion. The mean operative time was 142.18 ± 49.91 minutes (150.84 ± 50.32 minutes for total thyroidectomy and 110.20 ± 32.4 for lobectomy with isthmusectomy). The mean intraoperative blood loss was 20.45 ± 10.89 mL. The postoperative stay was 5.42 ± 1.49 days. The postoperative complication rate was 7.78%, including transient hypocalcemia in 30 patients, transient recurrent laryngeal nerve palsy in 3 patients, and skin ecchymosis in 9 patients.

Conclusions:

An understanding of crucial anatomical landmarks for clinical applied anatomy may improve the quality and safety of trans-areolar ET and subsequently help promote the development of ET.

Introduction

Thyroid diseases are common in women. Conventional open thyroidectomy is a safe and effective treatment. However, a scar with a length of 6–10 cm remains on the neck, imposing a substantial level of social and psychological stress on the patients.¹ The first endoscopic thyroidectomy (ET) was reported by Hüscher et al.² in 1997. ET has been described as an appropriate surgical alternative to conventional thyroidectomy in the past 20 years.^3,4 Although the safety and cosmetic results of ET have been confirmed, the learning curve for ET is still long.^5,6 Various studies have reported postoperative complication rates of 11.5%–40.9% for ET.^7–9 Excellent surgical technique is necessary for surgeons to improve the quality and safety of ET.

Certain anatomical landmarks exist in some surgical procedures. Clinical applied anatomy is helpful in promoting safe resection by reducing the operative time and surgical complications.^10,11 Clinical applied anatomy for trans-areolar ET is rarely discussed in the current literature. This study summarizes and describes the crucial anatomical landmarks for clinical applied anatomy in trans-areolar ET, which would help further enhance the quality and safety of trans-areolar ET.

Materials and Methods

Five hundred forty patients who underwent trans-areolar ET from January 2015 to June 2018 were enrolled in this study. The inclusion criteria for patients were as follows: (1) a diameter of benign thyroid nodules or follicular adenoma ≤5 cm, (2) hyperthyroidism of at least degree III, and (3) differentiated thyroid carcinoma without extraglandular invasion and lateral cervical lymph node metastasis. The exclusion criteria were as follows: (1) patients with a poor general condition who were unable to tolerate general anesthesia, (2) patients with severe coagulation disorders, and (3) patients with a history of neck surgery or irradiation. Institutional Review Board approval was obtained. All the patients provided written informed consent.

Preoperative blood tests included assessments of thyroid function, the intact parathyroid hormone level, serum Ca²⁺ level, and coagulation function. All patients underwent ultrasonography, a computed tomography scan, and a trachea softening test. Vocal cord movement was evaluated using a laryngoscope. Some patients with a preoperative suspicion of malignancy underwent fine needle aspiration. Patients with hyperthyroidism took a compound iodine solution for at least 2 weeks before surgery. Permanent recurrent laryngeal nerve (RLN) palsy or hypoparathyroidism was defined as nonimprovement within 6 months postoperatively.¹²

Surgical technique

The surgical procedure was performed according to the published literature.⁶ The dissection proceeded based on clinical applied anatomy during the operation and included the crucial anatomical landmarks listed as follows.

The subcutaneous superficial fascia

The placement of trocars is the first step of trans-areolar ET. Importantly, the trocars must be inserted in the correct anatomical layer. The subcutaneous superficial fascia is located between the adipose tissues and skin. The trocars were inserted below the subcutaneous superficial fascia and above the adipose tissues (Fig. 1).

FIG. 1.

The subcutaneous tunnel (A, the subcutaneous superficial fascia).

The suprasternal space

The superficial layer of the deep cervical fascia consists of continuous fibrous tissues that completely wrap the neck. At approximately the level of the seventh cervical vertebra, the superficial layer splits to form the suprasternal space with the anterior and posterior leaflets, attaching to the anterior and posterior proximal borders of the manubrium sterni.¹³ The loose connective tissues and anterior jugular vein are present in the suprasternal space (Fig. 2).

FIG. 2.

The suprasternal space (A, the loose connective tissues; B, the anterior jugular vein).

The sternocleidomastoid muscle

The sternocleidomastoid muscle originates at the manubrium of the sternum and the clavicle, and has an insertion at the mastoid process of the temporal bone of the skull. The sternocleidomastoid muscle is one of the anatomical landmarks that assists with the dissection (Fig. 3).

FIG. 3.

The sternocleidomastoid muscle and the linea alba cervicalis (A, the sternocleidomastoid muscles; B, the linea alba cervicalis; C, the infrahyoid muscles; D, the thyroid gland).

The linea alba cervicalis

The infrahyoid muscles consist of sternohyoid, omohyoid, sternothyroid, and thyrohyoid muscles. The inner edges of these muscles fuse into the midline of the infrahyoid muscles, which is called linea alba cervicalis (Fig. 3).

The trachea

The trachea consists of cartilage, smooth muscle, and fibrous tissues. The trachea was exposed by dissecting the lamina pretrachealis under the isthmus of the thyroid gland. In the absence of euangiotic blood vessels in the pretracheal space, the isthmus of thyroid gland was excised safely along the trachea (Fig. 4).

FIG. 4.

The trachea (A, the trachea; B, the isthmus of the thyroid gland).

Berry's ligament

Berry's ligaments are located on each side of the trachea. They extend from the cricoid cartilage or tracheal ring to the posteromedial aspect of each thyroid lobe. Berry's ligament is different from the anterior suspensory ligament that extends from the superior-anterior medial aspect of each thyroid lobe to the cricoid and thyroid cartilages.¹⁴ The RLN generally passes from the dorsolateral side of Berry's ligament, and thus this region must be dissected carefully to preserve the RLN (Fig. 5).

FIG. 5.

Berry's ligament (A, Berry's ligament; B, the thyroid gland; C, the trachea).

The parathyroid gland

Patients generally present with four parathyroid glands, including paired superior and inferior glands. Each gland typically weighs 35–40 mg, measures 3–8 mm in diameter, and varies in color from light yellow to reddish brown.¹⁴ The parathyroid glands should be distinguished from adipose tissues and lymphoid tissues (Fig. 6).

FIG. 6.

The parathyroid gland (A, the inferior parathyroid gland; B, the superior parathyroid gland; C, the thyroid gland; D, the trachea).

The RLN and the inferior thyroid artery

The RLN loops around the aorta or the right subclavian artery, then ascends through the tracheoesophageal groove behind the thyroid gland, and finally enters the larynx. The RLN is usually exposed in the Simon triangle that is formed by the common carotid artery laterally, the esophagus medially, and the inferior thyroid artery (ITA) superiorly. Three basic types of structures between the RLN and the ITA have been identified, including the nerve anterior to the artery, nerve between branches of the artery, and nerve posterior to the artery (Fig. 7).^15,16

FIG. 7.

The RLN and the ITA (A, the RLN; B, the ITA; C, the thyroid gland; D, the trachea). ITA, inferior thyroid artery; RLN, recurrent laryngeal nerve.

Results

Five hundred forty patients, including 108 men and 432 women, successfully underwent trans-areolar ET without conversion. The mean age of the patients was 39.95 ± 13.09 years (range: 16–82 years) (Table 1).

Table 1.

Clinical Features of the 540 Patients Who Underwent Endoscopic Thyroidectomy

Endoscopic thyroidectomy (n = 540)
Gender (n)
Male	108 (20.0%)
Female	432 (80.0%)
Age (years)^a	39.95 ± 13.09 (range: 16–82)
Pathological type (n)
Benign	407 (75.4%)
Malignant	133 (24.6%)

Value is presented as the mean ± standard deviation.

Postoperative pathology revealed nodular hyperplasia in 319 patients, follicular adenoma in 26 patients, Graves' disease in 57 patients, lymphocytic thyroiditis combined with thyroid nodules in 5 patients, papillary thyroid carcinoma in 128 patients, follicular carcinoma in 4 patients, and a malignant potentially undetermined tumor in 1 patient (Table 1).

Four hundred twenty-five patients underwent total thyroidectomy (TT), and 115 patients underwent lobectomy with isthmusectomy (LTIT). The mean operative time for the 540 patients was 142.18 ± 49.91 minutes (range: 21–355minutes), including 150.84 ± 50.32 minutes (range: 55–355 minutes) for TT and 110.20 ± 32.4 minutes (range: 21–228 minutes) for LTIT. The mean intraoperative blood loss was 20.45 ± 10.89 mL (range: 9–60 mL). The mean amount of drainage was 119.14 ± 60.16 mL (range: 0–410 mL). The mean postoperative hospital stay was 5.42 ± 1.49 days (range: 2–18 days) (Table 2).

Table 2.

Surgical Outcomes of the 540 Patients Who Underwent Endoscopic Thyroidectomy

Endoscopic thyroidectomy (n = 540)
Type of thyroidectomy (n)
TT	425 (78.7%)
LTIT	115 (21.3%)
Operation time (minutes)^a	142.18 ± 49.91 (range: 21–355)
TT	150.84 ± 50.32 (range: 55–355)
LTIT	110.20 ± 32.4 (range: 21–228)
Blood loss (mL)^a	20.45 ± 10.89 (range: 9–60)
Postoperative complication (n)	42 (7.78%)
Transient hypocalcemia	30 (5.56%)
Permanent hypocalcemia	0
Transient RLN palsy	3 (0.56%)
Permanent RLN palsy	0
Skin ecchymosis	9 (1.67%)
Tracheal injury	0
Infection	0
Amount of drainage (mL)^a	119.14 ± 60.16 (range: 0–410)
Postoperative hospital stay (days)^a	5.42 ± 1.49 (range: 2–18)

Values are presented as the mean ± standard deviation.

LTIT, lobectomy with isthmusectomy; RLN, recurrent laryngeal nerve; TT, total thyroidectomy.

The postoperative complication rate was 7.78%, including transient hypocalcemia in 30 patients, transient RLN palsy in 3 patients, and skin ecchymosis in 9 patients (Table 2).

Discussion

ET is a preferred alternative for patients with thyroid disease. The advantages of trans-areolar ET include the loose connective tissue, low skin tension, concealed scars, less scar hyperplasia, and greater convenience for bilateral resection.^17,18 However, the operative time is a potential limitation. The learning curve plays an important role in reducing the time of the ET operation.^6,19,20 The operative time for ET may be significantly longer than conventional open thyroidectomy during the early stage of the learning curve, resulting in additional costs and risks. In our study, the mean operative times for TT and LTIT were 150.84 ± 50.32 minutes and 110.20 ± 32.4 minutes, respectively, values that were less than some other reports.^12,21

The quality and safety of trans-areolar ET are related to the proficiency of the surgeon in the surgical approach and anatomical landmarks. The surgical approach is a primary condition established at the beginning of the procedure. The identification of the correct anatomical layer helps avoid unnecessary postoperative complications, such as subcutaneous hemorrhage and skin ecchymosis. The subcutaneous superficial fascia of the areola, the suprasternal space, and the sternocleidomastoid muscle are the key features used to determine the correct approach. The trocars should be inserted below the subcutaneous superficial fascia and above the adipose tissues, which is easily separated from the loose connective tissue. Mammary tissue damage may occur if the trocars are inserted too deep; meanwhile, the subcutaneous vessels may be injured if the trocars are inserted too shallow. Both the injection of inflation liquid (mixture of 1 mg of epinephrine and 500 mL of physiological saline) and a subcutaneous blunt dissection stick help the surgeon insert the trocars into the correct anatomical layer. In the suprasternal space, the loose connective tissues were dissected with an ultrasonic scalpel to establish the anterior cervical operation space. The tissues were separated along the anterior border of the sternocleidomastoid muscles and infrahyoid muscles. The skin flap was extended to the lateral edge of the sternocleidomastoid muscles, up to the superior edge of the thyroid cartilage, and down to the inferior edge of the suprasternal fossae.

The linea alba cervicalis, which is the midline of infrahyoid muscles, is able to be cut open by ultrasonic scalpel with little bleeding. It is an important landmark for the exposure of the thyroid gland. Before dissecting the glands, the isthmus and Berry's ligament were initially resected to obtain a larger working space. The isthmus was excised safely along the tracheal because the pretracheal space contains few blood vessels. The trachea was exposed by dissecting the false thyroid capsule under the isthmus. The trachea must be identified. The functional surface of the ultrasonic scalpel should be facing away from the trachea to avoid heat injury. No tracheal injury occurred in our study.

RLN palsy is one of the common complications of thyroid surgery that affects the quality of life of patients.^7,9 The anatomical relationship and variation must be mastered by surgeons to protect the RLN.¹⁶ According to Jung et al.,²² the incidence of RLN palsy is 2.9%, and RLN is found at the level of ITA, but significant individual differences in the relationship between the RLN and ITA were identified. Flament et al.²³ reported that the proportions of patients in which the RLN was located before, after, and between the ITA were 19.45%, 30.2%, and 50.35%, respectively, indicating a substantial variation in the anatomical relationship between the RLN and ITA. Three cases of transient RLN palsy were observed in our study. Based on our experience, Berry's ligament represents a useful anatomical marker to expose the RLN. The posterior suspensory ligament was described as Berry's ligament by Berry²⁴ in 1888, and then it was redefined as the lateral thyroid ligament by Serpell.²⁵ As shown in the study by Mohebati and Shaha,¹⁶ the RLN is usually located within 3 mm of the region of Berry's ligament, where RLN injury most frequently occurs. Berry's ligament is able to be completely dissected if the relationship between the RLN and the ligament is loose. In this situation, the gland is lifted outside the neck, and then the RLN is gently pushed away from the ligament. However, the nerve is difficult to expose if adhesion is observed between the RLN and Berry's ligament; therefore, parts of Berry's ligament and gland tissues should be retained in this case.

Hypocalcemia is a symptom of hypoparathyroidism. Its incidence ranges from 30% to 60% because of the use of different criteria to define the condition.²⁶ Thirty patients developed transient hypocalcemia in our study. Inadvertent parathyroidectomy and damage to the blood supply are the main causes of hypocalcemia. Familiarity with the anatomy of parathyroid glands is necessary to prevent inadvertent damage. Typically, four parathyroid glands are located on the posterior surface of the thyroid gland. They are either located in the thyroid capsule or thyroid parenchyma. Preservation of the parathyroid glands is usually achieved by a careful dissection in the thyroid capsule. The parathyroid glands should be separated gently from the thyroid gland.²⁷ After thyroidectomy, the thyroid specimens must be carefully examined, and then the inadvertently removed parathyroid glands can be reimplanted.

The mean intraoperative blood loss was 20.45 ± 10.89 mL in our study. Intraoperative bleeding mainly originated from thyroid vessels, the anterior cervical vein, and the subcutaneous vessels. Before excising the blood vessels, the ultrasonic scalpel was used to completely coagulate both the proximal and distal ends of the vessels, which enables more exact vascular closure. The functional surface of the ultrasonic scalpel must also face away from the parathyroid glands and RLNs to avoid subsidiary injury. Upon completion of the surgery, we routinely observed the presence of active bleeding in the subcutaneous operating space and the puncture tunnels before removing the endoscope. Bleeding in subcutaneous tunnels was treated with a percutaneous suture and pressure bandage.

We do not routinely dissect and expose the superior laryngeal nerve (SLN), because the probability of SLN injury is lower than injury to the RLN, and the exposure of additional anatomical structures may increase the probability of injury. The dissection should be performed close to the superior pole of the thyroid in the anatomical space between the superior thyroid vessels and the cricothyroid muscle to avoid SLN injury.

The postoperative stay was slightly longer than some reports. However, some objective explanations for this discrepancy are described as follows. First, the doctors and patients decided on a relatively conservative medical treatment due to the serious relationship between doctors and patients in our country. Both preferred a longer stay for safety. In addition, patients with underlying diseases underwent a detailed preoperative consultation with related departments before surgery and received comprehensive therapy after surgery. Second, most patients preferred to leave the hospital after the drainage tube was removed and they received the postoperative pathological report. We usually remove the drainage tube 2 days after surgery. The report of the postoperative pathological result requires 3–5 workdays to complete in our hospital. Third, the community health care system of our country is currently underdeveloped, and thus patients would rather stay in large modern hospitals for postoperative rehabilitation. Based on all these reasons, the postoperative stay of our patients was slightly longer.

The routine use of carbon nanoparticles and intraoperative nerve monitoring remains controversial.^28,29 Although an increasing number of reports suggest that these new methods help prevent subsidiary injury, their development is limited by the extra costs of monitoring equipment and materials, extra time required, and negative predictive values. The visualization of the RLN and the parathyroid gland is still the key to perform a safe ET.

An understanding of crucial anatomical landmarks for clinical applied anatomy in trans-areolar ET is useful to increase the safety, reduce the postoperative complications, and shorten the learning curve for surgeons. As surgeons gain experience, the application can be expanded to trans-areolar ET, and the development of other surgical approaches in ET will be promoted.

Footnotes

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

References

Lombardi

, Carnassale

, D'Amore

, et al. Morbidity from minimally invasive video-assisted thyroidectomy: A general review. Gland Surg, 2017; 6:488–491.

Hüscher

, Chiodini

, Napolitano

, et al. Endoscopic right thyroid lobectomy. Surg Endosc, 1997; 11:877.

Miccoli

, Berti

, Conte

, et al. Minimally invasive surgery for thyroid small nodules: Preliminary report. J Endocrinol Invest, 1999; 22:849–851.

Cho

, Park

, Baek

, et al. Single-incision endoscopic thyroidectomy for papillary thyroid cancer: A pilot study. Int J Surg, 2017; 43:1–6.

Kwak

, Kim

, Chae

, et al. Learning curve for gasless endoscopic thyroidectomy using the trans-axillary approach: CUSUM analysis of a single surgeon's experience. Int J Surg, 2014; 12:1273–1277.

Liang

, Hu

, Zhao

, et al. Learning curve for endoscope holder in endoscopic thyroidectomy via complete areola approach: A prospective study. Surg Endosc, 2015; 29:1920–1926.

Kim

, Kang

, Youn

, et al. Comparison of conventional thyroidectomy and endoscopic thyroidectomy via axill-bilateral breast approach in papillary thyroid carcinoma patients. Surg Endosc, 2016; 30:3419–3425.

Bellotti

, Capponi

, Cinquepalmi

, et al. MIVAT: The last 2 years experience, tips and techniques after more than 10 years. Surg Endosc, 2018; 32:2340–2344.

Yoo

, Chae

, Park

, et al. Comparison of surgical outcomes between endoscopic and robotic thyroidectomy. J Surg Oncol, 2012; 105:705–708.

10.

Perez

, São Julião

, Vailati

, et al. Lateral node dissection in rectal cancer in the era of minimally invasive surgery: A step-by-step description for the surgeon unacquainted with this complex procedure with the use of the laparoscopic approach. Dis Colon Rectum, 2018; 61:1237–1240.

11.

Singh

, Ohri

. Anatomic landmarks: Their usefulness in safe laparoscopic cholecystectomy. Surg Endosc, 2006; 20:1754–1758.

12.

Tae

, Ji

, Jeong

, et al. Comparative study of robotic versus endoscopic thyroidectomy by a gasless unilateral axillo-breast or axillary approach. Head Neck, 2013; 35:477–484.

13.

Casberg

. The clinical significance of the cervical fascial planes. Surg Clin North Am, 1950; 30:1415–1434.

14.

Loré

Jr.

Practical anatomical considerations in thyroid tumor surgery. Arch Otolaryngol, 1983; 109:568–574.

15.

Fancy

, Gallagher

D 3rd

, Hornig

. Surgical anatomy of the thyroid and parathyroid glands. Otolaryngol Clin North Am, 2010; 43:221–227.

16.

Mohebati

, Shaha

. Anatomy of thyroid and parathyroid glands and neurovascular relations. Clin Anat, 2012; 25:19–31.

17.

Liu

, Zhou

. A comparative study on the transareola single-site versus three-port endoscopic thyroidectomy. J Laparoendosc Adv Surg Tech A, 2017; 27:242–246.

18.

Tae

, Ji

, Song

, et al. Robotic and endoscopic thyroid surgery: Evolution and advances. Clin Exp Otorhinolaryngol, 2019; 12:1–11.

19.

Miccoli

, Berti

, Raffaelli

, et al. Comparison between minimally invasive video-assisted thyroidectomy and conventional thyroidectomy: A prospective randomized study. Surgery, 2001; 130:1039–1043.

20.

Cao

, Jin

, Cui

, et al. Learning curve for endoscopic thyroidectomy: A single teaching hospital study. Onco Targets Ther, 2013; 6:47–52.

21.

Lee

, Park

, Choi

, et al. Comparative study of a gasless transaxillary approach versus a bilateral axillo-breast approach for endoscopic thyroidectomy in a single institute. Head Neck, 2014; 36:702–708.

22.

Jung

, Park

, Ha

, et al. Endoscopic thyroidectomy using a gasless axillary approach. J Laparoendosc Adv Surg Tech A, 2007; 17:21–25.

23.

Flament

, Delattre

, Palot

. Anatomic pitfalls of recurrent laryngeal nerve dissection. J Chir, 1983; 120:329–333.

24.

Berry

. Suspensory ligaments of the thyroid gland. J Anat Physiol, 1888; 22:4–5.

25.

Serpell

. New operative surgical concept of two fascial layers enveloping the recurrent laryngeal nerve. Ann Surg Oncol, 2010; 17:1628–1636.

26.

Herranz GonZalez-Botas

, Lourido Piedrahita

. Hypocalcaemia after total thyroidectomy incidence, control and treatment. Acta Otorrinolaringol Esp, 2013; 64:102–107.

27.

Abboud

, Sleilaty

, Braidy

, et al. Careful examination of thyroid specimen intraoperatively to reduce incidence of inadvertent parathyroidectomy during thyroid surgery. Arch Otolaryngol Head Neck Surg, 2007; 133:1105–1110.

28.

Wang

, Su

, Xing

, et al. The function of carbon nanoparticles to improve lymph node dissection and identification of parathyroid glands during thyroid reoperation for carcinoma. Medicine (Baltimore), 2018; 97:e11778.

29.

Miller

, Spiegel

. Identification and monitoring of the recurrent laryngeal nerve during thyroidectomy. Surg Oncol Clin N Am, 2008; 17:121–144.