Relation of external branch of the superior laryngeal nerve and superior thyroid artery: a systematic review and meta-analysis

Introduction

The superior laryngeal nerve (SLN) arises from the inferior ganglion of the vagus nerve at the upper end of the carotid triangle (1). It gives off two branches, internal and external laryngeal branches within the carotid sheath. The internal laryngeal nerve is a sensory nerve which supplies the mucosa of the larynx above the vocal fold whereas the external branch supplies the cricothyroid muscle (1).

The superior thyroid artery (STA) is the first branch of the external carotid artery, arising just below the level of the greater cornu of hyoid bone which is located at the level of the third cervical vertebra. During its descent to supply the superior pole of the thyroid gland, it runs anterolateral to the external branch of the SLN (EBSLN) (2). The relationship of the EBSLN to the STA as per the classification of Cernea et al. is based on the distance between the intersection of the EBSLN, STA, and the superior pole. Type 1 nerves cross the STA either 1 cm or greater, above a transverse plane which passes through the upper border of the superior thyroid pole. Type 2a nerves cross the STA less than 1 cm above the plane, whereas type 2b nerves cross the STA beneath the plane (3,4).

Surgical procedures of the thyroid gland are associated with several complications, one of those being an injury to the EBSLN, due to its proximity to the superior pole of the thyroid gland (4). Thyroidectomy is the leading cause of injury to the EBSLN, while other surgical procedures that may cause harm to the EBSLN include neck dissection, carotid endarterectomy, excision of Zenker’s diverticula, and anterior cervical spine surgeries (5). The literature reports a range of 0 to 20% for the incidence of injury to EBSLN, with the majority of research citing a rate of less than 5% (6). Other literature has reported that iatrogenic injury to EBSLN can occur in as many as 58% of patients undergoing thyroidectomy (7-9).

Identification and preservation of the EBSLN is important as it is the only nerve that supplies the cricothyroid muscle (4). This muscle allows the vocal folds to lengthen and become thinner, raising the pitch of the voice (10). The vocal folds are tightened at frequencies above 150 Hz, which is why they are especially important for producing the high tones in the female voice range (11). The results of injury can cause atrophy, incomplete adduction, or bowing of the vocal cords leading to weakness of the voice and decreased range of pitch or volume (12,13). It can change the basic frequency of voice and impede the production of high tones (5,14). This can impair the quality of life and cause long-term morbidity, especially in women and individuals who depend on their voice professionally like singers and teachers (4,15). However, Cernea et al. observed that two patients had experienced a significant worsening of the complete range of voice performance, and not just affecting high tones (4). Uludag et al. also found evidence that the EBSLN contributes to the motor innervation of the cricopharyngeus muscle, which is the primary functional component of the upper esophageal sphincter and plays a crucial role in swallowing (16). Type 2 nerves, particularly type 2b, which is extremely vulnerable to a nerve lesion, are thought to be the nerves at an increased risk of an iatrogenic injury during a thyroidectomy (4). It has been noted in some studies that the size of the gland and toxicity are important factors in causing EBSLN injury. Ravikumar et al. and Menon et al. concluded that in high-volume glands of more than 50 cc, the incidence of type 2 nerve is common (7,17). The toxicity of the gland makes it more vascular and causes an increase in size. Type 2b nerves are common in toxic glands and type 1 in nontoxic glands (18). Because of this, identifying the EBSLN is essential to preventing injury.

It is important for the surgeon to start dissecting the superior thyroid pole by performing meticulous blunt dissection in the avascular plane between the medial aspect of the superior thyroid pole and the cricothyroid for good exposure of the EBSLN to minimize injury (19). Traction should be applied carefully in the lateral and caudal direction avoiding stretching of the nerve. Avoid unnecessary use of monopolar diathermy devices to control bleeding as heat transmission can cause nerve damage. Due to a wide variation in the course of the nerve and small diameter varying between 0.3 and 0.8 mm, it is important to identify and preserve the nerve before ligating the STA (10,20). To minimize injury, surgeons have embarked on various modalities such as utilization of neuromonitoring devices like Neurosign 100, and the use of endoscope as in video-assisted thyroidectomy which has a magnifying effect in visualizing the EBSLN (21,22).

In this systematic review, the prevalence of the EBSLN and the STA is identified in cadaveric studies and thyroid surgeries to prevent nerve injury. We present this article in accordance with the PRISMA reporting checklist (available at https://aot.amegroups.com/article/view/10.21037/aot-24-19/rc).

Methods

Search strategy

Relevant studies were searched in electronic databases of PubMed, Ovid Medline, and Science Direct by three different reviewers (F.H., H.H.A., and A.S.T.). Keywords and MeSH terms were used with Boolean operators: (“Superior laryngeal nerve”) OR (“External branch of the superior laryngeal nerve”) AND (“Superior thyroid artery”).

The search was restricted to studies published in English up until February 2024. The references of retrieved studies and related systematic reviews were manually checked for additional eligible studies that were not captured in the database search. Title, abstract, and full-text screening were performed independently by two reviewers. Any disagreement between the two investigators was resolved through discussion. The PRISMA flowchart indicating study selection is shown in Figure 1 (23).

Figure 1 PRISMA flowchart indicating study selection (23). EBSLN, external branch of the superior laryngeal nerve.

Study selection

Inclusion criteria

• Studies with cadaver;
• Intraoperative studies reporting the EBSLN and STA;
• Cernea classification.

Exclusion criteria

• Case reports;
• Letters to editors;
• Language (articles published in languages other than English).

The excluded studies were described in Table S1.

Data extraction

The two investigators (F.H. and I.A.S.B.) independently collected data from each study with the use of piloted data extraction sheets. Collected data were: first author, year of study, country of study, cadaver/patient (participants), and types of Cernea classification. Any disagreements were resolved by discussion with the third investigator (H.H.A.).

Study quality assessment

The two investigators (H.H.A. and A.S.T.) independently evaluated the methodological quality of eligible studies using the tool Anatomy Quality Assessment (AQUA) (Figure 2). This tool evaluates five domains: domain 1, objectives and subject characteristics; domain 2, study design; domain 3, methodology and characterization; domain 4, descriptive anatomy; and domain 5, reporting of results each domain has a set of signaling questions. For these signaling questions, “yes”, “no”, and “unclear” indicate a low, high, and unclear risk of bias, respectively (24). Domain 3 showed the highest percentage (69.6%) high risk of bias. Domain 5 had a 21.7% high risk of bias. The other domains showed a low risk of bias for included studies.

Figure 2 Risk of bias assessment by AQUA tools. AQUA, Anatomy Quality Assessment.

Statistical analyses

The pooled prevalence of each type of Cernea classification was calculated using the random effect model and presented with 95% confidence interval (CI). The Forest plot was used to depict the individual studies and pooled effect size. Heterogeneity was assessed with Tau-squared, which reflects the variance of true effect sizes, and I-squared statistic, which reflects the percentage of variation among true effect sizes not due to sampling error (25). A P value of less than <0.05 is indicative of a significant heterogeneity among the studies. Publication bias was assessed through funnel plot along with Eggar’s regression statistics. Sensitivity analysis was performed using sequential omission of individual studies in every comparison. All data were entered and analyzed using comprehensive meta-analysis software v.4, Biostat, Inc. (Englewood, NJ, USA).

Results

There are 23 studies across 14 countries that were eligible for the analysis of the prevalence of the EBSLN and the STA according to the Cernea classification. These studies were published between 1998 and 2022. Eleven studies were conducted with the cadavers (26-36) while the 12 studies were done with the patients during thyroidectomy (6,17,37-46). 21.7% and 17.4% of studies were done in Turkey and India respectively. 52.2% of the studies were done among patients. The number of examined nerves in each study ranged between 12 and 584 nerves in a single study. The main characteristics of the twenty-three included studies are provided in Table 1.

Prevalence

The forest plot depicts the individual studies and overall estimate of the prevalence. It is noticeable that the pooled prevalence of type 1 is 0.360 (Figure 3). Type 2a was shown to be prevailing at 0.329 (Figure 4). The pooled prevalence of type 2b was found to be 0.145 (Figure 5).

Figure 3 Pooled prevalence of Cernea type 1 nerves. CI, confidence interval.

Figure 4 Pooled prevalence of Cernea type 2a nerves. CI, confidence interval.

Figure 5 Pooled prevalence of Cernea type 2b nerves. CI, confidence interval.

Moderation analysis was done by analyzing studies on whether the data came from cadavers or patients. The prevalence of type 1 among cadavers was found to be 0.375 while among patients was 0.346 (Figure S1). For type 2a, the prevalence from cadaveric sources was 0.291 and 0.361 from patients. A prevalence of 0.128 of type 2b from cadavers seems lower than that from patients 0.160.

Heterogeneity

Table 2 shows the results of heterogeneity analysis using the random effect model. All studies involved in the analysis for each type of classification showed high heterogeneity which is significant at 0.005.

Sensitivity analysis

The forest plot for sensitivity analysis shows the overall computed prevalence when removing a particular study. Despite the P values being significant for all studies in type 1, there is no big change in the estimate when removing the study (Figure 6).

Figure 6 Sensitivity analysis (type 1 nerves). CI, confidence interval.

Similarly, for type 2a, sensitivity analysis showed a significant P value but with a minimal change in the overall estimate when removing a particular study (Figure S2).

Type 2b wasn’t an exception, similar results were found with minimal effect of removing studies.

Publication bias

The funnel plot for publication bias along with Eggar’s test showed that there was no evident publication bias among studies reporting types 1 and 2b. The funnel plot seems symmetrical, and Eggar’s test wasn’t significant. However, studies reporting data for type 2b seem to show some lack of symmetry in funnel plot and a significant Eggar’s test indicating some degree of publication bias (Table 3, Figure 7).

Figure 7 Funnel plot of standard error (type 2b nerves).

Discussion

This study examined the prevalence of EBSLN based on the Cernea classification which categorizes the nerve into type 1, type 2a, and type 2b. With a total pooled prevalence rate of 36%, type 1 Cernea nerves were found to be the most prevalent in the current study, followed by type 2a nerves at 32.9%. The least prevalent nerve type was type 2b, with an overall pooled prevalence rate of 14.5%. This study’s findings are consistent with those of others’ findings, including studies conducted by Cernea et al., Kierner et al., and Zhao et al., which found that type 1 nerves were most common, accounting for 60%, 42%, and 79.6% of cases, respectively (4,31,47). This stands in contrast to the findings of investigations conducted by Mishra et al., Aina and Hisham, and Ozlugedik et al., which reported greater incidences of type 2 nerve at 63.79%, 82.7%, and 60%, respectively (30,42,48).

In terms of cadaveric investigations, our present study showed that type I nerves were the most prevalent type (37.5%). Type 2a was the most prevalent kind in intraoperative studies, accounting for 36.1%. The type 2b was the least common with a prevalence of 12.8% and 16% in cadaveric and intraoperative procedures, respectively.

Despite that the results were stratified by whether the data came from cadavers or patients, the choice of random effect model is warranted in this review. In studies reporting an outcome from different parts of the region, variation is inevitable. This variation is related to the study setting, available resources, and the experience of the surgeon in identifying the target outcome.

The heterogeneity statistics affirm the presence of large variation between studies. It may reflect the presence of a confounding factor (49). Stratified analysis by source data (cadaver vs. patient) didn’t affect heterogeneity statistics significantly.

Nonetheless, this variation would be more relevant in comparative reviews which entail the calculation of pooled effect size to conclude favorable outcome. Sensitivity analysis didn’t identify any study with a significant impact on pooled effect size on omission.

There is strong evidence to support the theory that the higher prevalence of type 2 nerve course in intraoperative studies compared to cadaveric investigation is caused by an increase in thyroid volume brought on by a thyroid disease, which causes the superior pole of the thyroid to grow cranially and approach the EBSLN (43). Similarly, other investigators found that in their intraoperative investigation, type 2a nerves were the most commonly encountered. On the other hand, type 2b nerves were more common than type 2a nerves when they examined the EBSLN in massive goiters weighing more than 100 g (42). While examining large goiters, with an average thyroid mass of 430 g and lobe length of 10 cm, Cernea et al. found that type 2b EBSLNs were as common as 54% in nine individuals with 13 nerves at risk. Based on the volume of each lobe which is <20 mL (grade 1) and >20 mL (grade 2) Menon et al. (17) found type 2 nerve in high-volume glands. Ravikumar et al. (7) with a cut-off of 50 cc classified thyroid glands as small and large volumes and reported a higher incidence of type 2 nerve in large-volume glands (89.4%).

This suggested that the superior pole of the gland takes up a higher position in the neck and has a closer relationship with the EBSLN as it descends when the gland is noticeably enlarged (10,12).

In light of the findings, several precautions be taken to avoid injury to the EBSLN. It has been shown that studies using intraoperative neuromonitoring techniques had considerably higher EBSLN identification rates (95.90%) than those that just used direct visual identification (76.56%), resulting in the EBSLN going unnoticed and mistaken for fascia or connective tissue (8). Another study reported that nerve stimulators are especially beneficial in identifying type 1 nerves (50). Numerous surgical techniques have been proposed for the dissection of the thyroid gland’s superior pole. Bellantone et al. recommended that the STA be clamped as close to the gland’s capsule as possible and stressed the significance of exercising caution when performing the surgery (38). It has been suggested that the dissection of the capsule be performed in proximity to the medial surface of the thyroid’s upper pole (42).

In terms of ethnicity, one study showed that Malaysian Indians had a higher rate of type 2b nerves, which had nothing to do with the goiter’s size (29). In a similar vein, Cernea et al. discovered that non-White individuals exhibited a higher rate of type 2b nerves (41%) vs. White individuals (5%) (4). According to another study, the Mexican Mestizo population has a higher frequency of type 2 nerves (51). With this information, high-risk people may be more easily identified, and complications may be avoided by taking more safety measures.

Limitations

The published studies didn’t describe the surgical techniques or methods of identifying the anomalies. Most of the studies did not provide information regarding the expertise of the surgeons, although it plays a role in identifying the EBSLN. It is also interesting to note that, in addition, all surgeons did not routinely identify the EBSLN.

A lack of information on some variables that might affect the occurrence of the anomalies like ethnicity might pose a challenge in guiding surgeons.

Conclusions

Thyroid enlargement, ironically, is both a risk factor for damage to the EBSLN and one of the primary indicators for surgery. In view of a higher prevalence rate of type 2 nerves in intraoperative settings as compared to cadaveric studies, and particularly type 2b nerves in patients with enlarged thyroid glands, surgeons should be mindful in identifying and preserving the EBSLN to sustain voice function. Future research should compare various geographic regions because there is evidence of anatomical variations in EBSLN among ethnic groups. However, an enlarged thyroid gland seems to be a risk of injury since types 2a and 2b are higher, next to the thyroid. Consequently, the relation between the rate of paralysis of the criocothyroid muscle with type of EBSLN would be more relevant for future studies and demonstrate that types 2a and 2b increase the risk of paralysis of the cricothyroid muscle.

Acknowledgments

The authors would like to thank Dr. Mangala Kumari, an anatomist previously engaged with the Anatomy Department at IMU for contributing to this review.

Funding: None.

Footnote

Reporting Checklist: The authors have completed the PRISMA reporting checklist. Available at https://aot.amegroups.com/article/view/10.21037/aot-24-19/rc

Peer Review File: Available at https://aot.amegroups.com/article/view/10.21037/aot-24-19/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://aot.amegroups.com/article/view/10.21037/aot-24-19/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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