Feasibility of Doing a Safe Robotic Thyroidectomy in a Developing Country and Comparison of 2 Different Techniques

Abstract

This study aims to present our experience with robotic thyroidectomy approaches for differentiated thyroid carcinoma (DTC) vis a vis Modified BABA (Bilateral Axillo Breast Approach) and Retroauricular approach. Retrospective observational single institution-based study comprising 19 patients who underwent robotic thyroid surgery for DTC between October 2018 and January 2022. All patients underwent robotic thyroidectomy using the da Vinci Xi Robotic surgical system. Nineteen patients underwent robotic thyroidectomy with none needing conversion to open surgery. The Modified BABA approach was used for 9 patients (47%), whereas the Retroauricular approach (RA) was used for 10 patients (53%). In the RA group, 6 patients (60%) underwent total thyroidectomy and 4 patients (40%) underwent hemithyroidectomy. The Modified BABA approach was used for total thyroidectomy in 8 (89%) patients whereas 1 patient (11%) underwent hemithyroidectomy utilizing this approach. In 10 patients, central compartment clearance was done (5 through Modified BABA and 5 through RA). Lateral neck nodes were addressed in 4 patients (1 through Modified BABA and 3via RA). The median hospital stay was 4 days (range: 2–6 days). None of the 19 patients had post-operative complications like RLN palsy or any scar-related complaints /hypertrophic scars. The average PTH value post-op was 32.1 pg/ml (range: 3.8–70.4 pg/ml). Based on the current evidence from the literature, robotic thyroidectomy for thyroid carcinoma stands out from conventional surgery by resulting in sound oncological clearance with a superior cosmetic result by avoiding a scar in the anterior neck.

Introduction

The majority of thyroid carcinomas are associated with a good disease-specific prognosis, excellent overall survival, and significantly fewer cancer-related morbidities than other head and neck cancers [1]. Surgical approaches for thyroidectomy have seen a significant change in the past two to three decades, spanning from conventional transcervical thyroidectomy to minimally invasive thyroidectomy, endoscopic techniques and now, the present era of robotic approaches for thyroidectomy. Thyroid cancer tends to occur more in young female patients who are more cosmetically inclined, hence the evolutionary trend towards robotic approaches for thyroidectomy to reduce or hide the neck scar [2].

Chung, in 2007, was the first to use the da Vinci robotic system (Intuitive Surgical, Sunnyvale, California) for robotic transaxillary thyroidectomy [3]. Since then, robotic systems have been used all over the world with different approaches and various modifications such as Retroauricular (facelift), Trans-axillary, Bilateral Axillo-Breast, and Transoral [4–7]. The robotic system also helped overcome endoscopic surgery limitations, such as reduced range of motion and impaired eye-hand coordination. The basic fact that makes robotic thyroidectomy for thyroid carcinoma stand out from conventional surgery is sound oncological clearance can be achieved with a superior cosmetic result, as shown by different studies [8, 9]. Recently, the American Thyroid Association released its guidelines for robotic thyroidectomy, which shows a growing acceptance of this novel technology [10].

This study presents our initial challenges and experience at a tertiary cancer centre in a developing country with robotic thyroidectomies for DTC using Retroauricular and Modified Bilateral Axillo-Breast approaches, technical modifications and outcomes.

Materials and Methods

This retrospective observational study comprises 19 patients who underwent robotic thyroid surgery for differentiated thyroid carcinoma between October 2018 and January 2022 at Rajiv Gandhi Cancer Institute and Research Centre, New Delhi, India. Our institute is a high-volume tertiary cancer centre for thyroidectomies where we operate approximately 300 cases per year. On average, every 1 in 5 patients with thyroid carcinoma presenting to the head and neck oncology OPD inquires about robotic procedures but less than 20% of patients (50/300) were fit to undergo robotic thyroidectomy according to our selection criteria & out of that less than 40% could undergo robotic thyroidectomy due to the cost constraint in a developing country like India.

The preoperative diagnosis of patients with thyroid nodules was primarily determined by ultrasound examination, and all patients underwent fine-needle aspiration cytology (FNAC) preoperatively. Two patients had incidentally detected thyroid nodules on the whole-body [18 F] positron emission tomography scan. All patients underwent fiberoptic direct laryngoscopy to assess the vocal cords preoperatively.

All robotic thyroidectomies were performed using the Xi da Vinci Surgical system (Intuitive Surgical, Sunnyvale, California. In the last 2 years, we have used intraoperative nerve monitoring (IONM) using NIM III for all cases. The approach used was selected based on the extent of the disease, the patient’s preference, and the criteria mentioned below. Informed consent was obtained from all patients for robotic surgery.

The indications for robotic thyroidectomy were differentiated thyroid carcinoma of size not more than 4 cm in diameter without/with minimal extrathyroidal extension (ETE) and 1–2 cm without clinical-radiological evidence of ENE lymph node metastases in the central compartment or lateral compartment of the neck. Contraindications included large differentiated thyroid carcinoma with gross extra thyroid extension, bulky neck nodes with infiltration of adjacent neck structures, and a previous history of neck surgery. In our institution, either Modified BABA (Bilateral AxilloBreast Approach) or retroauricular approach (RA) for robotic thyroidectomy was used.

Selection Criteria of Various Approaches

A) Patients with nodules in both lobes of thyroid /nodule size not more than 4 cm/unilateral or bilateral central compartment nodes/ previous history of radiation therapy to the neck. These patients generally underwent a Modified BABA approach.

B) Patients with nodules between 3 and 4 cm in the thyroid lobe/nodes in the lateral compartment of the neck. These patients generally underwent a Retroauricular approach.

C) For patients who required total thyroidectomy with bilateral lateral compartment nodal clearance—a bilateral retroauricular approach was used.

D) Patients requiring hemithyroidectomy as per ATA guidelines were asked about personal preference for the approach.

E) Modified BABA was preferred as an approach for total thyroidectomy and even for unilateral/bilateral central nodal clearance. The retroauricular approach was mostly done if the lateral neck was to be addressed.

Our experience with robotic thyroidectomies over the last few years has resulted in this choice.

A) Modified BABA approach.

In this approach, we utilised five port incision sites, i.e., two breast (areola) ports, two axillary ports and one assistant port. The assistant port was always made on the right side between the breast and axillary port in the anterior axillary line, which the assistant used for suctioning, ligaclip application, and retraction of structures during surgery. All ports were 8 mm in length except the assistant port, which was 12 mm. The patient’s position was supine, with the neck extended and arms slightly abducted. Initially, laparoscopic-guided flap elevation with CO2 gas insufflation (6–8 mm Hg) using the right-sided ports, in a plane above the pectoralis muscle was done, and it took approximately 45 min using a laparoscopic 30-degree camera, cautery hook, and Sunction (initial port size −5 mm which was expanded before the robot was docked). Laparoscopic flap elevation was done till the thyrohyoid membrane superiorly, on the ipsilateral and contralateral side till the lateral border of SCM. Elevation of the flap in the ipsilateral supraclavicular fossa was also done. Medially flap was elevated approximately 3 cm across the parasternal area. Docking of the robot was done next, and robotic surgery commenced. The working space was maintained using CO2 insufflation at a pressure of 5–6 mm of Hg with a flow rate of around 15–16 l/min using the standard CO2 insufflator. The right breast port was used as the camera port (30 degrees). We used the left breast port for monopolar scissors (hot shear). Maryland bipolar was used in the right axillary port and Prograsp in the left axillary port.

The midline fascia between the strap muscles was divided, and the isthmus was dissected and cut initially to aid in mobilising the thyroid gland. The thyroid gland was dissected in the capsular plane, with preservation of the parathyroid glands, as well as the external branch of the Superior Laryngeal Nerve and Recurrent Laryngeal Nerve (RLN). Dissection was done from the inferior to superior aspect with dissection over the RLN done using Maryland bipolar and the current of the bipolar was decreased during dissection. The magnification allowed in the identification of the parathyroid gland blood supply and thus preserving its vascularity. In addition, the firefly mechanism of the da Vinci Robotic system was also used for parathyroid gland identification. The resected specimen was removed in a retrieval bag through the 12-mm assistant port. Suction drains were placed, haemostasis was done, and haemostatic agents (like fibrillar) were used and the port incisions were closed using subcuticular suture. Figures 1, 2, and 3 show surgical steps of Modified BABA.

Fig. 1.

(Modified BABA) patient position (neck extended) with surface markings and port incision marking

Fig. 2.

Port placement (C- camera port, HS- hot shears/harmonic scalpel port, PG- ProGrasp Forceps Port, MB- Maryland Bipolar Port, AP- Assistant port – Optional)

Fig. 3.

Docking of da Vinci Robotic Xi system from the head end in BABA

Advantages

1. Provides a symmetrical view similar to the conventional open surgery approach.

2. Gives the most significant operating angle to prevent instrument collision.

3. Both thyroid lobes and central compartment lobes can be easily approached.

4. The assistant port helps in retraction, suctioning, ligature-clips application and better handling of the gland.

5. Excellent cosmesis due to tiny separate and hidden port incisions.

Disadvantages

1) Requires a longer operative time.

2) Specimen retrieval of larger thyroid nodules is complex.

3) Difficulty in accessing lateral neck nodes, especially level II.

Tips and Tricks

1. Always make an assistant port. Larger-sized specimens can be retrieved by extending the assistant port minimally to 2–2.5 cm. The assistant port incision can also be used to re-implant the parathyroid gland in the Pectoralis Major muscle.

2. Laparoscopic flap elevation in our experience is not only faster but also results in fewer complications related to flap elevation as it is done under better vision and all minute bleeding points can also be cauterised.

3. Divide the isthmus initially for better mobilisation of the thyroid gland.

4. Capsular dissection should be done and individual branches of vessels should be cauterised

5. Hemostasis is to be done at lower pressure of CO2 insufflation – around 2–3 mm of Hg to identify the bleeders and haemostatic agents like fibrillar should also be used.

6. Ligaclip should applied at Level 4 on the left side to prevent a chyle leak.

Retroauricular Approach

This approach utilized the postauricular and occipital hairline incision. The flap was raised over the external jugular vein (EJV) and the greater auricular nerve (GAN) under direct vision and using a headlight as the platysma is deficient in this region. Caution should be maintained to avoid thinning of the flap. The tail of the parotid gland and platysma were then identified. The flap was then raised in the subplatysmal plane over the SCM muscle. Limits of raising the flap were the posterior border of the SCM muscle, superiorly to the lower border of the mandible, inferiorly up to the sternal notch and anteriorly to the anterior border of the contralateral SCM. The flap was raised posteriorly to the anterior border of the trapezius muscle if lateral neck dissection was also to be done. A small blade (Koh’s) of the Chung retractor was applied, and the robot was docked. The superior belly of omohyoid, sternohyoid and sternothyroid muscles were dissected and retracted using Prograsp to expose the thyroid gland. The parathyroid glands were identified and preserved. The Firefly mechanism of the da Vinci Robotic system was also used to identify the parathyroid glands. Cricothyroid muscle was identified and RLN was traced using cricothyroid muscle as a guide as it is found at the inferior border of the muscle usually entering the cricothyroid joint. RLN traced inferiorly in the tracheoesophageal groove and delineated. The Berry’s ligament was dissected, thyroid isthmus was cut and mobilised thyroidectomy was then completed. A suction drain was placed, and the incision was closed in layers. If total thyroidectomy was planned then the opposite strap muscle was mobilised, Prograsp was used to hold the opposite lobe and then inferior dissection was done to the superior pole. If visualisation is compromised then a preauricular incision can be given. Figures 4, 5, and 6 show the surgical steps of retro auricular approach and Fig. 7 shows RLN preservation during total thyroidectomy.

Fig. 4.

Retroauricular (RA) approach: skin incision marking (neck without extension); flap raised over scm

Fig. 5.

Raising skin flap while preserving greater auricular nerve (GAN)

Fig. 6.

External Retractors Chung’s Retractor or Dr. Koh’s retractor applied after flap raising and working space creation (minimum height – 3 fingers breadth/4 cm)

Fig. 7.

RLN (recurrent laryngeal nerve) preservation during robotic total thyroidectomy with CCND

Advantages

1. Closest approach to the thyroid; thus, operative time is less.

2. Good cosmesis, as the scar is hidden behind the auricle and hairline.

3. Approaching the lateral compartment neck nodes on the ipsilateral side is more accessible.

4. Larger thyroid nodules can be retrieved easily due to a longer incision.

Disadvantages

1. It does not provide a symmetrical view of thyroid surgery compared to the conventional approach.

2. Narrow working space leads to cluttering and collision of instruments.

3. Difficulty in accessing the contralateral lobe.

Tips and Tricks

1. Always place the incision within the hairline and increase the incision if visualization or a narrow tunnel (lack of working space) is a problem.

2. Use GAN, EJV, and SCM muscle as a guide initially for the correct plane of dissection.

3. Divide the isthmus initially for better mobilisation of the thyroid gland.

4. Superior to inferior dissection.

5. Ligaclip should applied at Level 4 on the left side to prevent a chyle leak.

6. Using three robotic instruments is better as Prograsp can be used for SCM retraction as well as IJV retraction during lateral neck dissection.

Bilateral Retroauricular Approach

This approach is similar to the ipsilateral Retroauricular approach, with the only addition of a contralateral postauricular incision for contralateral lobectomy/contralateral neck dissection when the exposure using the ipsilateral incision was inadequate.

Data Collection

In this retrospective review, data collection was done, which included patient and tumour characteristics, operative time, post-operative parathyroid hormone and ionised serum calcium levels, post-operative stay, histopathological results, number of retrieved lymph nodes, postoperative scar and Pre-Adjuvant radioiodine therapy Thyroglobulin levels. Total operative time was defined as the time from the first incision to the completion of skin closure, and it also included docking and undocking of the robot. Continuous variables were expressed as median with range, and categorical variables as numbers with percentage.

Results

The median age was 35 years (range, 21 to 49). Most patients were females (68%) whereas only 6 patients (32%) were male. All patients were of ECOG-0 status (100%). One patient (4%) had a history of receiving RT to the neck (Known case of Carcinoma Nasopharynx). Preoperative diagnosis showed papillary thyroid carcinoma (PTC) in 15 patients and follicular neoplasm in 4 patients. Out of 19 patients clinically, seven patients had PTC with nodules less than 1 cm (37%). In comparison, six patients had cT1b (31.5%) and the others had cT2 (31.0%) PTC. Also the aforementioned patients, 4 had multifocal disease in both lobes, while the rest had disease confined to the single thyroid lobe. Nine patients (47%) underwent thyroidectomy by the Modified BABA approach, whereas ten patients (53%) underwent thyroidectomy using the Retroauricular approach. In the Retroauricular approach, 6 patients underwent total thyroidectomy, and 4 patients underwent hemithyroidectomy. The Modified BABA approach was used in 8 patients for total thyroidectomy, whereas 1 patient underwent hemithyroidectomy by this approach. In 10 patients, central compartment clearance was done (5 through Modified BABA and 5 through the Retroauricular approach). Lateral neck nodes were addressed in 4 patients (1 through Modified BABA and 3 through Retroauricular); amongst these, a bilateral Retroauricular incision was given in 1 patient to address bilateral lateral compartment neck nodes. The median lymph node retrieval from the central compartment was six (2–15 nodes) and 51 nodes (22–108) from the lateral neck compartment. None of the patients needed conversion to open thyroid surgery. The median operative time was 240 min (range, 200 to 360 min), which was lower for the Retroauricular approach (approx. 200 ± 30 min) in comparison to Modified BABA (360 ± 35 min). The median hospital stay was 4 days (2 to 6 days).

Amongst the complications, 1 patient (5%) had temporary hypocalcemia, whereas another patient (5%) had seroma around the retro auricular suture line. None of the 19 patients had post-operative RLN palsy, and also none of the 19 patients had any scar-related complaints /hypertrophic scars. The average PTH value post-op was 32.1 pg/ml (range, 3.8–70.4 pg/ml). Pre-RAI scans Thyroglobulin levels were between 0.05 and 7.5 ng/ml. None of the patients had any unusual complications associated with robotic surgeries like brachial plexus injury, CO2 embolism or marginal mandibular nerve paresis. There was no post-operative mortality. Local or distant recurrence has not been seen in any patient till the present date with a minimum follow-up of 2 years. A detailed comparison of both approaches is listed in Tables 1 and 2. Figure 8 shows a post-op picture of the scar of the Retroauricular and Modified BABA approach at 6 months postoperatively.

Table 1.

Comparison of both approaches used in the study

Factors	Patients underwent Modified BABA approach N = 9 (47%)	Patients underwent Retroauricular approach N = 10 (53%)
Type of Thyroidectomy Hemi Total	1(11) 8 (89)	4(40) 6(60)
Central Compartment Clearance Yes No	5(55) 4(45)	5(50) 5(50)
Median Node Retrieval from Central Compartment	6.8	5.6
Lateral Neck Node Clearance Yes No	1(11) 8 (89)	3(30) 7(70)
Hypocalcemia -Temporary Yes No	0 (0) 9(100)	1(10) 9(90)
Hypocalcemia -Permanent Yes No	0 (0) 9(100)	0 (0) 10(100)
RLN palsy Yes No	0 (0) 9(100)	0 (0) 10(100)
Flap Edge Necrosis Yes No	0 (0) 9(100)	0 (0) 10(100)
Brachial Plexus Injury Yes No	0 (0) 9(100)	0 (0) 10(100)
Seroma Formation Yes No	0 (0) 9(100)	1(10) 9(90)
Haematoma Formation Yes No	0 (0) 9(100)	0 (0) 10(100)
CO2 Retention and associated complications Yes No	0 (0) 9(100)	0 (0) 10(100)
Chyle leak Yes No	1(11) 8 (89)	0(0) 10(100)
Median Operative Time	200 ± 30 min	360 ± 35 min
Conversion to open surgery Yes No	0 (0) 9(100)	0 (0) 10(100)
Mean Pre TG value before RAI	3.19	2.75
Scar related dissatisfaction according to patient Yes No	0 (0) 9(100)	0 (0) 10(100)
Recurrence Yes No	0 (0) 9(100)	0 (0) 10(100)

Table 2.

Comparison of both approaches used in the study

Factors	Modified BABA approach	Retroauricular approach
Nodule size  < 3 cm 3–4 cm	Equivalent Preferred	Equivalent
Type of Thyroidectomy Hemi Total	Equivalent Preferred	Equivalent
Central Compartment Clearance	Preferred
Lateral Neck Node Clearance		Preferred

Fig. 8.

Post-op 6 months photo of Robotic Retroauricular approach and Modified BABA approach

Discussion

The gold standard surgical approach for thyroidectomy in patients with thyroid cancer is the open conventional thyroidectomy. To establish any new novel approach, assessing its equivalence or improved outcomes is imperative, especially regarding rates of potential complications, financial expenditure, postoperative quality of life, and the ability to achieve standard goals of oncological surgical care [11, 12].

Many remote access approaches for thyroidectomy have been described to overcome unfavourable cosmetic outcomes of conventional open thyroidectomy [13, 14]. Robotic instruments overcome the limitations of endoscopic procedures, such as reduced range of motion, chopstick effect, rigid long instruments, and impaired hand–eye coordination (relying on 2D view). The Modified BABA approach which has an additional assistant port is otherwise technically similar to the robotic BABA approach described by KE Lee et al. [15]. A single-centre study of 260 patients by He et al. [16] showed a mean operative time (robotic BABA) of 201 ± 63 min, including a mean console time (of 80 ± 21 min). There was no implantation or metastasis in the chest wall or drain tract. Robotic BABA has disadvantages like longer operation time, use of CO2 insufflation, higher costs, and no haptic feedback. Insufflation of a high volume of CO2 (15 L/min) to maintain low pressure (5–6 mmHg) can obtain a satisfactory surgical field and avoid subcutaneous emphysema [17]. Despite our higher operative time, none of these complications has been seen in our study.

The other approach used in our study is the Retroauricular approach. Terris et al. [18] popularised the facelift incision for robotic thyroidectomy, demonstrating improved operative time compared to the transaxillary technique, which was a similar finding in our study when compared to the modified BABA approach.

In another study by Lira et al. [19], comprising 2,769 thyroid surgical procedures (2015–2017), 48 (1.7%) were robot-assisted (26 hemi-thyroidectomies, seven total thyroidectomies, 12 total thyroidectomies with selective neck dissection (II–VI), and three neck dissections for thyroid carcinoma). Transient marginal mandibular nerve paresis occurred in 4 (8.3%) patients but normalised at 1 month. No other major surgical complications were seen that were comparable to our data.

Seup Kim et al. [20] calculated direct & indirect costs for robotic Total Thyroidectomy with CCND and lateral ND in comparison to conventional Total thyroidectomy with CCND and MRND, with an observation of a statistically significant difference in costs, favouring the traditional approach ($13,608-Robotic vs. $4,704 open approach, p < 0.001). In our institute, the cost also favours the open approach ($5,374 Robotic vs. $ 3,364 open approach).

Due to a lack of studies that directly compare BABA/Modified BABA and Retroauricular approaches for total/hemi thyroidectomy, we have shared our experience using both approaches, especially in a developing country, their feasibility, and preferred indications for each approach. The drawback of this study is the small sample size with a retrospective analysis. To have a substantial implication, a more extensive sample-sized prospective study with a direct head-to-head comparison of both approaches to define their specific indications is advocated.

Thus, with recent studies and extensive data on Robotic Thyroidectomy worldwide, the American Thyroid Association published a statement in 2016 highlighting that remote-access thyroidectomy may be performed safely in high-volume centres. The statement acknowledged the role of robotic thyroidectomy in selected patients with strict selection criteria, promoting Robotic thyroidectomy as an acceptable approach in differentiated thyroid cancer [10]. The learning curve for this procedure has to be acknowledged. This will gradually decrease the complication rates and the operative time, thus achieving the goals of any successful robotic surgery.

Conclusion

In conclusion, our initial experience shows that robotic thyroidectomies can be safely performed even in developing countries. Based on the current evidence from the literature, robotic thyroidectomy for thyroid carcinoma stands out from conventional surgery by resulting in sound oncological clearance with a superior cosmetic result by avoiding a scar in the anterior neck. Both Modified BABA and Retroauricular approaches depend on the extent of disease, surgeon expertise and sometimes patient preference. The Retroauricular approach stands out regarding easier accessibility for lateral compartment clearance and the Modified BABA approach for Total thyroidectomy and central compartment clearance. Newer advancements with more affordable robotic systems, Indian surgical robotic system (SSI Mantra) becoming available, more experience using these and their application in head and neck surgery will further reduce the financial cost to the patient.

Declarations

Conflict of Interest

The authors declare no competing interests.