Surgeons use various techniques to identify the Recurrent Laryngeal Nerve (RLN) during operative procedures on the neck. These range in palpation, direct inspection, intraoperative nerve monitoring, and anatomical landmarks such as the suspensory ligament of the thyroid gland (Ligament of Berry, BL) and the Tracheoesophageal Groove (TEG). The BL is a fibrous structure that anchors the thyroid gland to the first three rings of the tracheal cartilage [
Anatomical location of the Berry Ligament.
The RLN is the structure most at risk for iatrogenic injury during procedures on the anterior neck, particularly thyroidectomy [
Reports of the location and relationship of the RLN to the BL and TEG have varied widely. The reported presence of an RLN coursing within the TEG has ranged from 24.9% to 100% [
The high rate of RLN injury, and the need to protect the structure during surgery, has motivated extensive research during recent years. However, a reliable and uniform method for isolating and safeguarding the nerve has yet to be formulated. Our intention is to provide a comprehensive evidence-based assessment, supplemented by our own cadaveric study, of the anatomical reliability of the BL and TEG as landmarks for identifying the RLN. Reliable landmarks would help to reduce the rate of iatrogenic injury and long term postoperative complications.
A total of 36 formalin-fixed cadavers were dissected bilaterally at the Department of Anatomy, Jagiellonian University Medical College, Krakow, Poland, to investigate the anatomical relationship of the RLN to the BL and TEG. A midline vertical incision was made starting from the mentum and continuing inferiorly to the sternal notch. The dissection was continued through the subcutaneous adipose tissue. Subplatysmal flaps were then raised. Next, the superior and inferior attachments of the sternohyoid and sternothyroid muscles were transected and the dissection was continued until the thyroid gland was visible. All surrounding muscles and adipose and connective tissues were then carefully removed. The RLN was visualized with the aid of medial traction on the trachea. The relationship of the nerve to the BL was recorded (superficial, piercing, or deep). The nerve was then traced inferiorly to the Tracheoesophageal Groove, and the position of the RLN with respect to this groove was recorded (inside or outside: anterior, anterolateral, lateral, and posterior).
The research protocol for this study was approved by the Jagiellonian University Medical College Ethics Committee (registry number KBET/319/B/2012). The study was performed in accordance with the ethical standards established in the 1964 Declaration of Helsinki and its later amendments.
Through August 2016, the major electronic databases PubMed, China National Knowledge Infrastructure (CNKI), ScienceDirect, EMBASE, BIOSIS, SciELO, and Web of Science were searched to identify potential studies for the meta-analysis. No date limits or language restrictions were imposed. The comprehensive PubMed search strategy is presented in Supplement 1 in Supplementary Material available online at
Studies were considered eligible for inclusion in the meta-analysis if they (1) reported clear, extractable prevalence data on either the relationship of the RLN to the BL or the relationship of the RLN to the TEG and (2) were cadaveric, intraoperative, or imaging studies. The exclusion criteria included (1) case studies, case reports, conference abstracts, and letters to the editor; (2) studies reporting incomplete data; and (3) studies of patients with trauma to the head and neck region.
Each study was independently assessed for eligibility by at least two reviewers. Any disagreements arising during this assessment were resolved by a consensus among the entire review team, after consultation with the authors of the original study, if possible. Full-text articles in languages not spoken fluently by the reviewers were translated for further eligibility assessment by medical professionals fluent in both English and the original language of the article.
Data from the included studies were independently extracted by two reviewers. The extracted data included year, country, type of study, study design, number of nerves, prevalence of the different types of relationships of the RLN to the BL (superficial, piercing, or deep) (Figure
Types of relationship between the Recurrent Laryngeal Nerve and the Berry Ligament.
Possible locations of the Recurrent Laryngeal Nerve in relation to the Tracheoesophageal Groove.
For the analysis of cadaveric data, prevalence rates and elements of descriptive statistics were used where appropriate. To pool the data into the meta-analysis, pooled prevalence estimates were calculated using MetaXL version 2.0 by EpiGear International Pty. Ltd. (Wilston, Queensland, Australia). A random effects model was used for all meta-analysis calculations. Heterogeneity among the included studies was measured using the Chi2 test and the
Subgroup analyses to explore potential sources of heterogeneity were based on type of study (cadaveric versus intraoperative), side (left versus right), and geographical distribution. Confidence intervals of the rates were used to investigate significant differences between subgroups, any overlap between two or more subgroups indicating a lack of statistical significance [
Among the 36 formalin-fixed cadavers dissected, 16 (44.4%) were men and 20 (55.6%) were women. The mean age was 68.9 ± 11.7 years. The RLN was identified bilaterally in all 36 cadavers (
Cadaveric data on the relationship of the Recurrent Laryngeal Nerve to the Berry Ligament.
Superficial: # (%) | Piercing: # (%) | Deep: # (%) | |
---|---|---|---|
Total | 65 (90.3%) | 5 (6.9%) | 2 (2.8%) |
Right | 33 (91.7%) | 2 (5.6%) | 1 (2.8%) |
Left | 32 (88.9%) | 3 (8.3%) | 1 (2.8%) |
Cadaveric data on the relationship of the Recurrent Laryngeal Nerve to the Tracheoesophageal Groove.
Inside TEG: # (%) | Outside TEG: # (%) | Outside- anterior: # (%) | Outside- anterolateral: # (%) | Outside- lateral: # (%) | Outside- posterior: # (%) | |
---|---|---|---|---|---|---|
Total | 49 (68.1%) | 23 (31.9%) | 2 (8.7%) | 4 (17.4%) | 17 (73.9%) | 0 (0.0%) |
Right | 26 (72.2%) | 10 (27.8%) | 2 (20.0%) | 1 (10.0%) | 7 (70.0%) | 0 (0.0%) |
Left | 23 (63.9%) | 13 (36.1%) | 0 (0.0%) | 3 (23.1%) | 10 (76.9%) | 0 (0.0%) |
A summary of the flow of studies through the meta-analysis is presented in Figure
PRISMA flow chart of study identification and inclusion in the meta-analysis.
A total of 16 studies (
Table of studies included in the Recurrent Laryngeal Nerve-Berry Ligament meta-analysis.
Study | Country | Type of study | | Berry’s Ligament | ||
---|---|---|---|---|---|---|
Superficial (%) | Piercing (%) | Deep (%) | ||||
Present study | Poland | C | 72 | 90.3 | 6.9 | 2.8 |
Asgharpour 2012 [ | England | C | 185 | 88.1 | 11.9 | 0 |
Berlin and Lahey 1929 [ | USA | I | 44 | 100 | 0 | 0 |
Berlin 1935 [ | USA | I | 140 | 75.0 | 25.0 | 0 |
Botelho et al. 2012 [ | Brazil | C | 41 | 61.0 | 19.5 | 19.5 |
Çakir et al. 2006 [ | Tukey | C | 130 | 100 | 0 | 0 |
Chen et al. 2008 [ | China | C | 100 | 0 | 5 | 95 |
Freschi et al. 1994 [ | Italy | I | 84 | 41.7 | 0 | 58.3 |
Hunt et al. 1968 [ | Australia | C | 151 | 47.0 | 0 | 53.0 |
Kaisha 2011 [ | Kenya | C | 121 | 67.0 | 7.4 | 25.6 |
Leow and Webb 1998 [ | England | C | 25 | 100 | 0 | 0 |
Ngo Nyeki et al. 2015 [ | Cameroon | I | 62 | 93.5 | 6.5 | 0 |
Pradeep et al. 2012 [ | India | I | 584 | 61.8 | 31.2 | 7.0 |
Sasou et al. 1998 [ | Japan | I | 486 | 100 | 0 | 0 |
Sunanda et al. 2010 [ | Sri Lanka | I | 45 | 55.5 | 6.7 | 37.8 |
Wade 1955 [ | Wales | I | 200 | 10 | 25 | 65 |
Subgroup analysis for relationship of the Recurrent Laryngeal Nerve to the Berry Ligament.
Number of studies (number of nerves) | Superficial: % (95% CI) | Piercing: % (95% CI) | Deep: % (95% CI) | | |
---|---|---|---|---|---|
Overall | 16 (2470) | 78.2 (51.5–90.8) | 7.0 (0–19.6) | 14.8 (0–33.0) | 99.1 (98.9–99.2) |
Cadaveric | 9 (965) | 77.6 (42.0–97.3) | 6.8 (0–26.5) | 15.5 (0–40.7) | 98.8 (98.5–99.1) |
Intraoperative | 7 (1505) | 76.0 (34.9–100) | 7.0 (0–32.3) | 17.0 (0–49.4) | 99.4 (99.2–99.5) |
Africa | 2 (183) | 83.4 (35.9–100) | 7.6 (0–44.2) | 8.9 (0–47.0) | 97.2 (93.0–98.9) |
Asia | 4 (1215) | 59.8 (0–100) | 8.4 (0–56.6) | 31.8 (0–89.5) | 99.6 (99.5–99.7) |
Europe | 6 (696) | 81.5 (35.0–100) | 5.3 (0–34.3) | 13.2 (0–50.1) | 99.1 (98.9–99.3) |
North America | 2 (184) | 90.7 (54.6–100) | 9.0 (0–45.4) | 0.3 (0–18.1) | 96.3 (89.9–98.6) |
Sensitivity (≥ 100 nerves) | 9 (2097) | 70.7 (32.1–92.4) | 9.0 (0–30.1) | 20.3 (0–46.7) | 99.4 (99.3–99.5) |
Forest plots for prevalence of Recurrent Laryngeal Nerve relationship pattern with respect to the Berry Ligament.
A total of 23 studies (
Table of studies included in the Recurrent Laryngeal Nerve-Tracheoesophageal Groove meta-analysis.
Study | Country | Type of study | | Tracheoesophageal groove | |
---|---|---|---|---|---|
Inside (%) | Outside (%) | ||||
Present study | Poland | C | 72 | 68.1 | 31.9 |
Al-Salihi and Dabbagh 1989 [ | Iraq | C | 212 | 83.0 | 17.0 |
Altorjay et al. 2009 [ | Hungary | I | 1023 | 39.4 | 60.6 |
Ardito et al. 2004 [ | England | I | 1856 | 64.4 | 35.6 |
Armstrong and Hinton 1951 [ | USA | C | 40 | 60.0 | 40.0 |
Asgharpour et al. 2012 [ | England | C | 197 | 33.0 | 67.0 |
Berlin 1935 [ | USA | I | 140 | 65.0 | 35.0 |
Bowden 1955 [ | England | C | 55 | 89.1 | 10.9 |
Chen et al. 2002 [ | China | C | 90 | 100 | 0 |
Freschi et al. 1994 [ | Italy | I | 84 | 67.9 | 32.1 |
Hisham and Lukman 2002 [ | Malaysia | I | 491 | 47.0 | 53.0 |
Hunt et al. 1968 [ | Australia | C | 151 | 70.2 | 29.8 |
Iqbal and Zubair 1998 [ | Pakistan | I | 93 | 77.4 | 22.6 |
Jiang et al. 2008 [ | China | I | 292 | 45.9 | 54.1 |
Jing et al. 2007 [ | China | C | 100 | 85 | 15 |
Lang et al. 1986 [ | Germany | C | 43 | 37.2 | 62.8 |
Lang et al. 1986 [ | Germany | C | 146 | 34.2 | 65.8 |
Lu et al. 2012 [ | China | I | 79 | 76.0 | 24.0 |
Menck et al. 1990 [ | Germany | C | 202 | 24.3 | 25.7 |
She et al. 1984 [ | China | C | 200 | 37.0 | 63.0 |
Skandalakis et al. 1976 [ | USA | C | 204 | 48.5 | 51.5 |
Uen et al. 2006 [ | Taiwan | C | 120 | 85.0 | 15.0 |
Zhang and Cheng 2011 [ | China | C | 80 | 90.0 | 10.0 |
Subgroup analysis for relationship of the Recurrent Laryngeal Nerve to the Tracheoesophageal Groove.
Number of studies (number of nerves) | Inside TEG: % (95% CI) | Outside TEG: % (95% CI) | | Cochran’s | |
---|---|---|---|---|---|
Overall | 23 (5970) | 63.7 (55.3–77.7) | 36.3 (28.3–44.7) | 97.4 (96.8–97.9) | <0.001 |
Cadaveric | 15 (1912) | 65.8 (50.7–79.5) | 34.2 (20.5–49.3) | 97.7 (97.1–98.2) | <0.001 |
Intraoperative | 8 (4058) | 60.1 (49.9–70.0) | 39.9 (30.0–50.1) | 97.0 (95.7–97.9) | <0.001 |
Asia | 10 (1757) | 75.9 (60.2–88.9) | 24.1 (11.1–39.8) | 97.8 (97.0–98.4) | <0.001 |
Europe | 9 (3678) | 50.9 (38.0–63.7) | 49.1 (36.3–62.0) | 97.7 (96.8–98.3) | <0.001 |
North America | 3 (384) | 57.5 (45.4–69.1) | 42.5 (30.9–54.6) | 78.8 (32.3–93.3) | 0.009 |
Right | 10 (1597) | 62.1 (48.1–75.2) | 37.9 (24.8–51.9) | 95.3 (93.2–96.8) | <0.001 |
Left | 10 (1554) | 68.0 (56.4–78.6) | 32.0 (21.4–43.6) | 93.4 (21.4–43.6) | <0.001 |
Sensitivity (≥ 100 nerves) | 14 (5334) | 54.9 (45.3–64.3) | 45.1 (35.7–54.7) | 97.6 (97.0–98.2) | <0.001 |
Forest plots for the pooled prevalence of the Recurrent Laryngeal Nerve location with respect to the Tracheoesophageal Groove.
Ten studies (
Subgroup analysis for position of a Recurrent Laryngeal Nerve located outside the Tracheoesophageal Groove.
Number of studies (number of nerves) | Anterior: | Anterolateral: | Lateral: | Posterior: | | Cochran’s | |
---|---|---|---|---|---|---|---|
Overall | 10 (1268) | 45.7 (1.1–81.1) | 6.0 (0–32.0) | 37.4 (0–72.1) | 10.9 (0–40.7) | 99.4 (99.2–99.5) | <0.001 |
Cadaveric | 7 (531) | 47.0 (0–82.0) | 7.5 (0–36.6) | 26.1 (0–62.6) | 19.5 (0–54.8) | 98.8 (98.5–99.1) | <0.001 |
Intraoperative | 3 (737) | 41.7 (0–100) | 2.7 (0–100) | 54.2 (0–100) | 0.4 (0–100) | 99.5 (99.3–99.6) | <0.001 |
Europe | 7 (1098) | 23.0 (0–61.6) | 3.3 (0–28.6) | 59.8 (6.1–93.9) | 13.9 (0–49.3) | 99.3 (99.1–99.4) | <0.001 |
North America | 3 (170) | 85.6 (46.5–100) | 10.4 (0–42.1) | 0.6 (0–16.5) | 3.3 (0–26.2) | 95.3 (89.6–97.9) | <0.001 |
Right | 5 (515) | 38.0 (0–100) | 3.2 (0–47.2) | 50.7 (0–100) | 8.1 (0–60.7) | 99.0 (98.7–99.3) | <0.001 |
Left | 5 (433) | 27.1 (0–76.5) | 6.3 (0–44.4) | 56.7 (0–100) | 9.9 (0–52.1) | 98.5 (97.8–99.0) | <0.001 |
Sensitivity (> 100) | 4 (1051) | 35.7 (0–100) | 0.8 (0–100) | 42.7 (0–100) | 20.8 (0–100) | 99.7 (99.6–99.8) | <0.001 |
Anatomical landmarks such as the BL and TEG come with caveats of which surgeons need to be cognizant before using them in the operating theater.
In our cadaveric dissections, there was a 90.3% prevalence of the RLN coursing superficially to the BL. This coincides with the prevalence rates noted in studies such as those by Asgharpour et al. (2012) and Ngo Nyeki et al. (2015) [
Symmetrical RLN patterns with respect to the BL were noted in most cases (80.6%) in our dissections. This information is useful for surgeons performing total thyroidectomies, in that once one nerve is identified, the same location should be assessed first on the contralateral side. The RLN/BL relationship was similarly symmetrical in our meta-analysis: 75.5% of nerves behaved the same on both sides.
Our dissections revealed that the TEG is a somewhat less reliable landmark, only 68.1% of nerves coursing within the groove. This is very similar to the 63.7% pooled prevalence estimate of nerves coursing within the TEG obtained from the meta-analysis. The meta-analysis and cadaveric study differed with regard to the location of the RLN when it was outside the TEG. It was most commonly (73.9%) located lateral to the TEG in our cadavers, but most RLNs outside the TEG (45.7%) were found anteriorly in the meta-analysis. Differences aside, RLNs were found largely, if not exclusively, in locations ranging from anteriorly to laterally. All RLNs in our cadaveric study and 89.1% of cases in our meta-analysis lay within this range. Subgroup analysis of the RLN/TEG relationship revealed no statistically significant differences. Small differences were noted between the cadaveric (34.2%) and intraoperative (39.9%) accounts of those nerves found outside the TEG. We posit that pathologies resulting in these operative procedures, such as large multinodular goiters, slightly alter the physiological location of the RLN. This subanalysis revealed geographical differences, Asian studies generally reporting more RLNs coursing in the TEG (75.9%) than European ones (50.9%). Assessment of RLN/TEG behavior in our cadavers confirmed that the symmetrical pattern of the course (61.1%) was slightly less common than the symmetrical behavior of the RLN with respect to the BL.
The BL has been considered one of the most reliable landmarks in neck surgery [
The TEG is a valuable landmark for identifying the RLN. It provides some shelter, inside which the nerve can be overlooked, but simple palpation of it can provide valuable information about the presence of the RLN [
Additional research in this area is needed for a number of reasons. Future clinical trials need to be conducted to assess the intraoperative viability of the BL and TEG as landmarks for identifying the RLN, primarily through assessing the prevalence of iatrogenic RLN injury. Establishment of the BL and TEG as truly significant markers for at-risk neural structures requires further prospective studies of high power and sound methodology.
This meta-analysis was limited by several factors: in particular, the studies did not report the location of the RLN with respect to the TEG uniformly. This restricted the overall analysis to the distinction “inside or outside the TEG” rather than a more detailed assessment such as inside, anterior, anterolateral, posterolateral, and posterior. Two separate analyses could be completed on these variables, but they cannot be compared to each other. Moreover, the high heterogeneity among studies persisted despite substantial subgroup analysis, suggesting it could be attributed to intrinsic population variability in prevalence. Further limiting factors included the lack of any quality assessment and risk-of-bias tool for anatomical studies, and a lack of assessment of publication bias, as no statistical measure is currently available for anatomical prevalence meta-analysis. Throughout the study, the original authors were contacted when necessary and available in attempts to resolve discrepancies, provide clarification, and minimize bias.
The use of anatomical landmarks for identifying structures intraoperatively is valuable in many procedures, including those in the neck. The BL and TEG are both essential for performing complication-free thyroidectomies. The BL proved the more reliable of the two landmarks with 78.2% of RLNs coursing superficially to it. The TEG was slightly less consistent, with 68.1% of nerves found within the groove. The development of a uniform and consistent procedure, such as identifying the RLN in the TEG and tracing it upwards to the BL for confirmation, will help to preclude iatrogenic injuries and avoid complications. The confirmation of reliable landmarks on which to base those procedures is the first step in that process.
The authors declare no conflict of interests.
This study was supported using the statutory funds of the Jagiellonian University Medical College. Krzysztof A. Tomaszewski was supported by the Foundation for Polish Science (FNP). We wish to thank Karolina Saganiak for the anatomical drawings used in this manuscript. The publication of this manuscript was supported by the Faculty of Medicine, Jagiellonian University Medical College KNOW (Leading National Research Centre 2012–2017) funds.