Introduction

Background

Thyroidectomy is a quite common daily operation in general surgery and it requires detailed anatomical information. The thyroid gland is a butterfly-shaped endocrine organ located in the anterior compartment of the neck at the level 5th cervical to 1st thoracic vertebrae1,2,3. The recurrent laryngeal nerve (RLN) runs near the thyroid gland and is at risk during thyroid and parathyroid surgery4. The RLN most commonly courses within the tracheoesophageal groove (50–77%), but it may also be found in the paratracheal region (17–40%), the paraesophageal area (6%), or embedded in the thyroid parenchyma (4%); it frequently divides into two or three branches before entering the larynx5. The anatomical structures of the region, mainly the relationship of recurrent laryngeal nerve and inferior thyroid artery (ITA) make the procedure challenging6.

The Non-Recurrent Laryngeal Nerve (NRLN) is a rare anatomical variant, commonly associated with an aberrant right subclavian artery (ARSA), or arteria lusoria, with an incidence of 0.6–1.3% on the right side, which may increase with intraoperative neuromonitoring. This anomaly arises from an embryologic malformation of the aortic arch, where the right subclavian artery originates from the left side of the arch in the absence of brachiocephalic trunk, and coursing behind the esophagus. This can cause dysphagia lusoria due to compression of the esophagus. Recognizing this association preoperatively can help predict NRLN and prevent injury during surgery. The NRLN may rarely be on the left side in cases of dextrocardia or situs inversus, with an incidence of 0.04%7,8,9.

During thyroidectomy, the RLN is at risk of iatrogenic injury which is one of the major complications of thyroid surgery resulting in significant postoperative patient morbidity. RLN injury and transient post-operative RLN paralysis occur in approximately 3–8% of cases whereas permanent paralysis occurs in 0.3–3% of cases. Therefore, identifying the anatomical variant of RLN does have significant importance in preserving the nerve and its function during surgery. Although recent monitoring advances have allowed intraoperative neuromonitoring to reduce the incidence of RLN injury, visual identification of the RLN remains the gold standard for RLN injury prevention10.

The RLN is vulnerable to compression, traction, and transection due to the diminished caliber of the nerve and its anatomical variations. Variations in the RLN can be produced by changes in the course of the nerve due to previous surgery or the impaction of a mass, the relationship between the RLN and inferior thyroid artery (ITA), the nonrecurrent laryngeal nerve course, and extra laryngeal branching. The RLN typically branches superior to the inferior thyroid artery and posterolaterally to the ligament of Berry. This anatomical relationship is important to consider during thyroid dissection4,11.

Surgeons should be familiar with the variations in RLN topography and the technique for preserving trunk and terminal branches of RLN to decrease the risk and enhance the safety of thyroid surgery12. The 3 main identification approaches for RLN dissection include the lateral, inferior, and superior approaches. During thyroidectomy, the RLN may divide into anterior and posterior branches. The anterior branch lies close to the thyroid capsule, whereas the posterior branch is positioned further away. If only the posterior branch is identified, the anterior branch is at higher risk of injury during capsular dissection. Identifying the anterior branch first, however, usually allows the surgeon to find the posterior branch as well, thereby reducing the likelihood of injury. Injury to the anterior branch is particularly important because it carries a high risk of vocal cord palsy and long-term complications11.

The incidence of RLNI is higher during re-explorations, Graves disease, and thyroid carcinoma procedures10. Despite the incidence rate of NRLN being rare, the probability of intraoperative injury can reach 12.9%13. Thus, consideration and recognition of every variation is essential to minimizing the rate of RLN injury during thyroid surgery. The American Association of Endocrine Surgeons and ATA Guidelines for the definitive surgical management of thyroid disease recommended that RLNs should be identified and preserved during dissection in thyroid operation14.

Even though thyroidectomy is one of the most common procedures performed by General Surgeons, in the presence of several anatomical variations, there is little known regarding the anatomical variations of RLNs encountered in Ethiopia. Being the first study in our country, this study will reveal the real anatomical variations of RLN, using inferior identification approach with inferior thyroid artery as a consistent anatomical landmark, in our region and lay the groundwork for future studies.

Methods and materials

Study area and period

This study was conducted at Tibeb Ghion Specialized Hospital (TGSH) in Bahir Dar, Ethiopia, from June 2021 to August 2022. The hospital, located 550 km northwest of Addis Ababa, is a tertiary-level healthcare facility that provides specialized care to patients from the Amhara region and beyond.

Study design

This was an institutional-based prospective observational study of consecutive patients who underwent thyroidectomy with RLN dissection and preservation at Tibebe Ghion Specialized Hospital between June 2021 and August 2022. A non-probability consecutive sampling technique was used to enroll all eligible patients during the study period. Data (intraoperative findings and early postoperative outcomes) were recorded prospectively by the operating team using a standardized checklist and intraoperative photographs.

Data collection procedure

Patients having thyroid neoplasm or thyroid-related disorder and who met the inclusion criteria undergone thorough preoperative evaluation and investigations, and written informed consent was taken. Later patients underwent the planned type of thyroidectomy, which included dissection, identification, and preservation of the RLNs using the inferior approach with ITA as a consistent anatomical landmark. The operating team completed the checklist, including relations with important neck anatomic structures like ITA, trachea, TEG, Zuckerkandl tubercle and parathyroid glands, after the procedure and took intraoperative photographs of the RLNs from the inferior pole of the thyroid gland to the cricothyroid membrane. These data were recorded immediately after each operation by the operating team (resident/operating surgeon) and verified daily by the principal investigator, confirming that data collection was prospective. These photographs, along with the completed checklist, were used to analyze the study outcomes. The checklist was developed based on a review of similar studies and adapted to the local context. The collected data is on sociodemographic characteristics, type of thyroidectomy, laterality, early postoperative outcomes, intraoperative transfusions, intraoperative accidents, comorbidities, duration of surgery, indications, and anatomic variations. Resident physicians and ward nurses were involved in data collection, with daily supervision by the principal investigator to ensure completeness and accuracy of the data.

Inclusion and exclusion criteria

The study included patients who underwent thyroidectomy with dissection, identification and preservation of RLNs. Patients who underwent repeat anterior neck surgery; those who already had RLN palsy before the surgery; those who underwent completion thyroidectomy or previous neck dissection; those with unclear intraoperative pictures of the RLN; or those with intraoperative RLN involvement were not included.

Results

Sociodemographic characteristics

A total of 102 consecutive patients were included in this prospective observational study. The tested population in this prospective study consisted of 92 women and 10 men with 53.9% between 18 and 39 years of age. A total of 156 laryngeal nerve dissections, including 69 on the left side and 87 on the right side, were performed with unilateral exposure in 48 patients and bilateral exposure in 54 patients. The most common type of thyroidectomy performed was subtotal thyroidectomy, 80.4%, followed by total thyroidectomy (14.7%) and near total thyroidectomy (4.9%) with controlled toxic multinodular goiter (CTMNG) being the most common indication, 64.7%, followed by simple nodular goiter (SNG) with compressive symptoms (15.7%), thyroid cancer (13.7%) and thyroid neoplasm (5.9%). Most of the patients were from rural part of the country, 83.3% and 95.1% were orthodox Christianity followers [Tables 1 and 2].

Table 1 Postoperative thyroidectomy patients’ information who had undergone laryngeal nerve dissection at Tibeb ghion Hospital, June 2021 to August 2022.
Table 2 Sociodemographic characteristics of thyroid patients who had undergone laryngeal nerve dissection at Tibeb ghion Hospital, June 2021 to August 2022.

Branching patterns of RLN

The findings indicated that RLN has several variations based on the branches it gives and its relation with ITA and TEG. On the right side, 24.1% (18.4% bifurcations and 5.7% trifurcations) demonstrated branching of the RLN and 10.2% demonstrated branching (bifurcations) on the left side [Table 3]. Using the Fisher’s Exact Test, and following data analysis, it was determined that there is a statistically significant difference in the branching pattern between the two sides. There were no patients with a non-recurrent laryngeal nerve anatomic variation. Figures 3 and 1, and 2 show intra-operative images of the recurrent laryngeal nerve demonstrating its branching patterns as a single trunk, and with two and three extra-laryngeal branches, respectively.

Table 3 Frequency distribution of RLN branching pattern in thyroid patients who had undergone laryngeal nerve dissection at Tibeb ghion Hospital, June 2021 to August 2022.
Fig. 1
figure 1

Intra-operative image of RLN with two extra-laryngeal branches.

Fig. 2
figure 2

Intra-operative image of RLN with three extra-laryngeal branches.

Fig. 3
figure 3

Intra-operative image of single trunk RLN.

Relation of RLN with ITA and TEG

The relationship between RLN and ITA, a common landmark used by surgeons to locate RLN during thyroidectomy, was also examined. In relation to ITA, 68.9% of right RLN’s were related posteriorly, while 27.7% were related anteriorly. On the left side, 91.3% of RLNs were posterior to ITA whereas 7.3% were related anteriorly. The anatomical variation of RLN which interdigitate between branches of ITA were demonstrated in 3.4% and 1.4% on the right and left sides respectively [Table 4]. There is statistically significant difference between the two sides, as determined by P < 0.05 (Fischer’s Exact Test).

Table 4 Frequency of relationship of RLN to the ITA in thyroid patients who had undergone laryngeal nerve dissection at Tibeb ghion Hospital, June 2021 to August 2022.

The relation of RLN with another important landmark during thyroidectomy, TEG, was also examined. On the right, 93.1% of RLNs ran within the tracheoesophageal groove (TEG) and 6.9% lay lateral to the trachea; no lateral placement was observed on the left.

Early postoperative outcome

Of all the patients included in this study 92.2% had uneventful early postoperative period, in the first seven days after thyroidectomy, with hoarseness and hypocalcemia (symptomatic patients with serum calcium < 8.5 mg/dl postoperatively) occurred in 2% of the cases each and there was one death with immediate cause of death of upper airway obstruction.

Associated comorbidities were identified in 13.7% of the patients with hypertension being the most common, 12.7%, which could be due to the fact that most, 54%, of the patients were less than 40 years of age [Table 5]. Intraoperative transfusions were required only in two patients with intraoperative accident, vascular, occurred only in a single case and 73.5% of thyroidectomies were completed within two hours.

Table 5 Early Postop outcome and comorbidities in patients who had undergone laryngeal nerve dissection at Tibeb ghion Hospital, June 2021 to August 2022.

Discussion

In this prospective observational study, the anatomical variations of RLNs in patients who underwent thyroid surgery were examined. The traditional course of RLNs is as follows: the left RLN separates from the vagus nerve hooking around the aortic arch and returns into the larynx in the TEG. In comparison, the right RLN originating from the vagus nerve travels below the subclavian artery before entering the larynx within the TEG. The nerve passes posterior to ITA before it ascends in the neck. However, not every RLN follows the same above course. Many publications have described various arrangements of RLNs and techniques for identifying and protecting RLN during thyroid surgery.

In this study several anatomical variations of RLN were identified based on branching pattern and it’s relation with important anatomical landmarks during thyroid surgery, ITA and TEG. Extralaryngeal branching of the RLN is the most common anatomical variation encountered during thyroidectomy. We have observed branching of the RLN in 24.1% on the right side compared to 10.2% on the left side which is within the range of figures reported from studies done in Chinese patients whereas it is lower than those studies done on cadaver dissection from US12,15,16. It was suggested that observing branching of RLN is underestimated in intraoperative studies on live patients. In addition, it was determined that there’s a statistically significant difference in the branching pattern between the two sides.

In addition to the branching, RLN has variations based on the course it takes in relation to ITA and it was observed that more anterior course of the nerve occurred on the right side, with a more anterolateral course, compared to the left side which is similar to the results reported in studies done in China and US, even if the magnitude is lower in this study. Similarly, we have observed a more lateral course of the RLN on the right side compared with the left side, which has a more consistent course in the TEG, similar to the results reported in the previous studies.

In addition to the greater number of branches, the relationship of the right RLN to the ITA and TEG may potentially make it more vulnerable to injury as well compared to the typical relation between RLN and ITA/TEG, where the RLN passes posterior to ITA in the TEG16. It was observed that a significantly higher rate of anatomical variations of the right RLN compared with the left RLN.

Most of the patients who underwent thyroidectomy had uneventful early postoperative period, 92.2%, and hoarseness and hypocalcemia were the most common morbidities observed in this study, 2% each. It was also demonstrated that these morbidities occurred in patients who underwent total thyroidectomy with the duration of surgery being greater than 2 h.

Limitations of the study

The study population comprised only patients who underwent thyroid surgery, resulting in a male-to-female ratio of 1:9 and therefore the observed anatomical variations of the RLN were more frequent among female patients. The study period was relatively short and the sample size was small.

Conclusion and recommendations

Conclusion

The anatomical variations of RLN are frequently encountered in patients who undergo thyroid surgery. The large anatomical variability of RLN may increase the risk of vocal cord paralysis caused by RLN injury. The awareness of these anatomical variations of RLN by surgeons may be helpful in the dissection, identification and preservation of the nerve with its terminal branches for a safe thyroidectomy. It is advisable that all branches of the RLN need to be identified and then preserved during thyroidectomy, especially in a setup like ours, where it is not the routine practice.

Recommendations

Surgeons should be aware of the possible anatomical variations of the RLN that may be encountered during thyroid surgery, and dissection, identification, and preservation of the nerve should be a routine practice during thyroidectomy. Future multi-institutional studies including more male patients and incorporating long-term follow-up are recommended to determine whether variations of the nerve increase the risk of iatrogenic injury. Measurement of anthropometric characteristics such as gland size, neck circumference, and BMI, as well as pre- and postoperative laryngoscopic evaluation, should be considered in future studies. Moreover, further comparative prospective studies comparing the outcomes of thyroid surgeries performed with and without identification and preservation of the RLN are warranted.