Between January 2011 and April 2023, 2205 thyroid surgeries were performed at Tsuchiya General Hospital, including 512 total thyroidectomies, 850 right hemithyroidectomies, 761 left hemithyroidectomies (LHT), and 82 complementary total thyroidectomies. Out of a total of 2717 inferior laryngeal nerves at risk, NRILNs were identified in 12 asymptomatic cases (0.44% overall, 0.86% of the right nerves), which involved two men and ten women (Table 1). In all patients, the anomaly involved the right laryngeal nerve. In case 9, LHT + D1 central lymphadenectomy was performed for papillary thyroid carcinoma in the left lobe of the thyroid gland. NRILNs on the right side were confirmed by dissection of the right III lymph node. In eight cases, the non-recurrent laryngeal nerve originated from the vagus nerve and descended into the larynx with the superior pole of the thyroid lobe (Type 1), whereas in four cases, it crossed in close proximity to the inferior thyroid artery (Type 2). In all cases, preoperative CT confirmed ARSA, and cervical US revealed loss of the normal bifurcation of the right common carotid artery and right subclavian artery. Surgery was initiated based on the preoperative diagnosis of NRILN in all cases. IONM, which was introduced in our hospital in 2019, allowed the detection of NRILNs during thyroid surgery in five cases. No nerve lesions or postoperative vocal-fold deficits were observed in any patients.
The abnormal formation of the subclavian artery during fetal development is implicated in the pathogenesis of NRILN [7]. The heart, which is located in the neck during early fetal development, descends into the thoracic cavity as fetal development progresses. Under normal conditions, the right subclavian artery is formed from the right fourth aortic arch, and the ductus arteriosus is formed from the left sixth branchial arch. The laryngeal nerve withdraws into the thoracic cavity as the heart descends. Then, the nerves present as the recurrent nerves that turn around the right subclavian artery and aortic arch, respectively. However, when the right fourth aortic arch is abnormally lost in the early embryonic stage, an ARSA is formed by a compensatory seventh intersegmental artery [15]. As a result, the right inferior laryngeal nerve does not pass into the thoracic cavity and branches directly from the cervical vagus nerve without forming a recurrent loop [22]. The ARSA most commonly follows a retroesophageal course (80–84%), which is between the trachea and esophagus (12.7–15%), or a pretracheal course (4.2–5%) [11, 12]. NRILN mostly occurs on the right side, occurring on the left side only when there is a situs inversus or right aortic arch [7]. Only six cases of left NRILN have been reported [5].
The incidence of this abnormality ranges from 0.3–1.6% in the right non-recurrent laryngeal nerve. However, the exact incidence is difficult to determine because few surgical reports are available [20]. A series of more than 1000 published cases is summarized in Table 2, with incidence rates ranging from 0.34–1.04% [1, 3, 4, 6, 7, 10, 13, 14, 17, 20]. Although NRILNs occur infrequently, head and neck surgeons may often encounter this variation, and preoperative detection is important. Deveze et al. [4] reported 104 patients with NRILNs showing abnormally running arteries, emphasizing the need to consider the presence of NRILNs in these patients. Satoh et al. reported that the sensitivity and specificity of CT for detecting NRILN are both 100% (abnormalities of the right subclavian artery were noted in all 10 NRILN cases in 1086 patients who underwent preoperative CT), indicating the usefulness of preoperative CT [14]. Iacobone et al. have found that the preoperative performance of US to identify arterial abnormalities significantly decreases NRILN morbidity. Demonstrating the absence of the brachiocephalic trunk, with the right carotid artery arising from the aortic arch independently and separated from the right subclavian artery, is a more rapid and easier method than direct identification of the origin of the aberrant lusorian artery from the left side of the aortic arch because of its deep location. The absence of the brachiocephalic artery predicts NRILN with a sensitivity and negative predictive value of 100% and a specificity of 97.7% [8, 9]. However, the positive predictive value for NRILN due to the absence of the brachiocephalic artery on US has been reported as 45.9% [8]. In cases where the right brachiocephalic artery branches from the central side (closer to the aortic arch), evaluating the absence of branching of the right brachiocephalic artery using US angled caudally at the sternal notch may be insufficient. Prior to the present study, we encountered one case in which the absence of the brachiocephalic artery could not be detected by preoperative US, and NRILN was found intraoperatively. Therefore, in addition to preoperative cervical US, all patients underwent CT, which revealed abnormalities in the running of the artery, thus predicting the presence of NRILNs in our hospital.
F: female, M: male, PTC: papillary thyroid carcinoma, CTT: completion total thyroidectomy, TT: total thyroidectomy, RHT: right hemithyroidectomy, LHT: left hemithyroidectomy, STT: subtotal thyroidectomy, D1: central lymphadenectomy, RASA: right aberrant subclavian artery.
Table 2
Incidence of nonrecurrent inferior laryngeal nerve in large published series
Author
|
Year
|
Number of operations
|
Number of NRILN
|
Frequency
(%)
|
Stewart [8]
|
1972
|
1776*
|
6
|
0.34
|
Henry [5]
|
1988
|
6307***
|
33
|
0.52
|
Proye [9]
|
1991
|
6961***
|
56
|
0.80
|
Defechereux [10]
|
2000
|
2517***
|
20
|
0.79
|
Deveze [11]
|
2003
|
19868***
|
104
|
0.52
|
Toniato [7]
|
2004
|
6000**
|
31
|
0.51
|
Satoh [12]
|
2013
|
1561*
|
11
|
0.70
|
Gong [13]
|
2014
|
1825**
|
23
|
1.26
|
Barcynzki [14]
|
2015
|
2500**
|
9
|
0.37
|
Le [15]
|
2019
|
2158**
|
16
|
0.74
|
This study
|
2023
|
1402*
|
12
|
0.86
|
* Number of right recurrent nerves identified at surgery |
** Number of thyroidectomies |
*** Number of neck explorations (cervicotomies) |
However, the course of non-RLNs may vary. Two main types are defined by Cangnol et al. [2], Toniato et al. [20], and Sugino et al. [18]. Henry et al. [7] have classified the types as superior, middle, or inferior based on the nerve running pattern. Le et al. [10] have identified a V-shaped type and classified the four traveling patterns. Toniato et al. [20] have classified NRILNs as Type 1 (from the superior pole) or Type 2 (from the inferior pole). We followed the classification reported by Sugino et al. in 1998 [18], in which Type 1 is defined as the inferior pole and Type 2 as the superior pole. The ratio of cases involving Type 1 to Type 2 branching from the lower branching level has been reported as 26:7 by Henry et al. [7], 26:5 by Toniato et al. [20], 6:1 by Satoh et al [14], 10:2 by Le et al. [10], and 5:2 by Terao et al. [19], indicating a higher incidence of branching from the lower pole level. Similarly, in this study, Type 1 bifurcation from the lower pole was more common than Type 2 bifurcation from the upper pole (eight vs. four patients, respectively). Toniato et al. [20] have reported a higher incidence of nerve damage in cases with branching from the superior pole (three out of five cases). Even if preoperative identification of NRILN is possible, the specific running pattern cannot be predicted. Therefore, comprehensive vascular treatment of the upper pole of the thyroid gland should be carefully performed, focusing on the branches of the superior thyroid artery along the thyroid gland capsule.
NRILN, encountered in approximately 1% of thyroid surgeries, is not extremely rare. In many cases, NRILNs are injured during the early stages of perithyroid dissection. Literature indicates that RLN injury occurs in approximately 3–7% of patients following thyroid surgeries, while the incidence of NRLN injury may reach as high as 12.9% [10].
To minimize the risk of damaging NRILN and ensure safer surgical procedures, the following measures are recommended: (1) preoperative evaluation of ARSA via US and CT; (2) not dissecting the nerve-like tissue that enters the superior pole of the right lobe from the lateral side during surgery on the right lobe of the thyroid gland until the right recurrent nerve is identified; (3) if the right recurrent nerve is not easily identified, the carotid sheath and cervical vagus nerve should be exposed and carefully examined to determine the presence of NRLN leading toward the thyroid gland; and (4) after confirming the presence of the right recurrent nerve, right lobectomy should be performed.