Level VI lymph nodes : an anatomic study of lymph nodes located between the recurrent laryngeal nerve and the right common carotid artery

1 University of Sao Paulo, Faculty of Medicine, Human Structural Topography Discipline, Sao Paulo, SP, Brazil. 2 Santa Casa de São Paulo, Medical Sciences Faculty, Medicine Course, Sao Paulo, SP, Brazil. Saleh Level VI lymph nodes: an anatomic study of lymph nodes located between the recurrent laryngeal nerve and the right common carotid artery. 2 Rev Col Bras Cir 45(6):e1972 It is worth mentioning that the surgical approach of this space causes greater morbidity due to the syntopy of the structures of the RCR and of the lymph nodes located there, as there is a necessity to mobilize the right recurrent laryngeal nerve in order to remove the fibro-fatty tissue that contains the lymph nodes. This study aims to verify the presence of lymph nodes in the region located among the right common carotid artery, the right inferior thyroid artery, and the right recurrent laryngeal nerve, to describe them, and to evaluate if there is a correlation between anthropometric factors and these studied lymph node characteristics.


T his work describes a specific region not yet
reported in anatomy compendiums.The territory in question is locatedamong the right recurrent laryngeal nerve, the right common carotid artery, and the right inferior thyroid artery, and we called it Recurrent Carotid Recess (RCR).We can discuss its clinical importance taking as an example the carcinoma of the thyroid gland, including all its subtypes.This is the most common malignant endocrine neoplasia in humans, and its prevalence showed a steady and accentuated increase in the last three decades 1 .
When there are metastases of this primary site, the lymph nodes are the main compromised organs.The perivisceral lymph nodes are located in the central compartment of the neck, defined as level VI, which is delimited laterally by the common carotid arteries, inferiorly by the jugular notch, and superiorly by the hyoid bone 2 , and that coincides with the muscular triangle, described in the anatomy compendiums.
The reason for the existence of a differentiated territory in this triangle or compartment has its bases in anatomy: the recurrent laryngeal nerve on the right, bypassing inferiorly the right subclavian artery, penetrates the central compartment of the neck, far from the tracheoesophageal groove, which does not occur on the left.Thus, the right recurrent laryngeal nerve divides the paratracheal lymph nodes into two compartmental groups: one anterior and the other posterior.This posterior region, whose location is hidden, may be the site of metastases 3 .

Linfonodos do nível VI: estudo anatômico dos linfonodos localizados entre o nervo laríngeo recorrente e a artéria carótida comum direita.
It is worth mentioning that the surgical approach of this space causes greater morbidity due to the syntopy of the structures of the RCR and of the lymph nodes located there, as there is a necessity to mobilize the right recurrent laryngeal nerve in order to remove the fibro-fatty tissue that contains the lymph nodes.
This study aims to verify the presence of lymph nodes in the region located among the right common carotid artery, the right inferior thyroid artery, and the right recurrent laryngeal nerve, to describe them, and to evaluate if there is a correlation between anthropometric factors and these studied lymph node characteristics.Each corpse was then placed in the horizontal dorsal decubitus position with the head in hyperextension position.An incision was made in the anterior aspect of the thorax in the horizontal direction towards the two acromions.This incision extended to the superficial cervical fascia.From this plane, the myocutaneous flap was elevated in the cranial direction up to the level of the thyroid cartilage.After this step, a vertical incision was made in the midline of the superficial and pre-tracheal cervical fascia, exposing the thyroid gland.This incision extended from the thyroid cartilage to the jugular notch.The dissection extended between the thyroid gland and the sternohyoid and sternothyroid muscles on the right, with the bending of these muscles laterally.With this maneuver, the territory between the right carotic sheath and the trachea was exposed, individualizing the thyroid gland, and, through a thorough dissection of this region, the area to be studied (RCR) was exposed.In this way, the following structures were visible: inferior thyroid artery (upper limit), recurrent laryngeal nerve, common carotid artery, brachiocephalic trunk (lateral and inferior border), pre-vertebral fascia, and esophagus, in the deep plane, as well as, in some cases, the right cervical pleura (Figure 1).All the fibro-fatty tissue located in this space was resected in bloc (Figure 2) and each one received identification with its own numbering (from 01 to 32) and its respective SVOC-FMUSP identification number.This material was fixed for 24 hours in 10% buffered formaldehyde, with pH between 7.2 and 7.4.After this period, the piece was transferred to a sequence of increasing concentration of alcoholic solutions (70%, 80%, and 90%), remaining for seven days at each concentration.The material was then placed in Xylol solution for nine days.After this period, the specimen was transferred to a methyl salicylate solution, remaining for seven days.At the end of this process, the specimen was analyzed for lymph node count and for photographic recording with a digital camera (Figure 3).Microscopic evaluation of lymph nodes was performed after hematoxylin-eosin staining, and all histological slides were analyzed by a single investigator using an optical microscope.2).

METHODS
The significant relationship between race and the presence of lymph nodes (p=0.04) was also demonstrated (Table 3).

Race
Study conducted at the Faculty of Medicine of Universidade de São Paulo (USP), in the Human Structural Topography Discipline, and approved by the Ethics Committee under the number 203/16.Thirty-two adult cadavers, with a maximum post-mortem interval of 24 hours, of both genders, and of different ethnicities and biotypes, were included in this study.Previous cervical surgical manipulation and head and neck neoplasms were exclusion criteria.The corpses came from the Death Verification Service of the Medical School of Universidade de São Paulo (SVOC-FMUSP), Brazil.Initially, demographic data (such as gender, age, and race), as well as anthropometric data (such as biotype, height, and weight), were collected and recorded in a specific table.
The macroscopic evaluation of the lymph nodes found in the RCR in relation to the number and to the longitudinal (greater axis) and transversal (smaller axis) diameters was performed, using a digital caliper.Data were included in a specific table.
Numerical variables were described by number of lymph nodes and dimensions associated with the standard deviation.The 95% confidence interval (CI) was calculated considering the presence of level VI lymph nodes, according to Wilson's method.The nominal variables were described by frequency (%).Fisher's exact test was used to correlate anthropometric data with the presence or absence of lymph nodes in this region.The correlation of these data was calculated by the Spearman's test.We considered alpha of 0.05 and a study power of 80%, using the Stata v14 program (StataCorp.2015.Stata Statistical Software: Release 14. College Station, TX: StataCorp LP).RESULTS Data related to the demographic characteristics of the sample studied here are described in table 1, which shows the characteristics of age, gender, weight, height, race, and anthropometric data (short, medium-height, and tall individuals), recorded in this study population.In this work, there was predominance of mediumheight white males.The dissection indicated the presence of lymph nodes in 22 (68.75%) of the 32 cadavers with 95%CI (15.19-47.31).In cases where they were found, the mean was 1.56±0.29 lymph nodes per cadaver.The relationship between the presence of lymph nodes and medium-height specimens (p=0.03) was observed (Table

Figure 2 .
Figure 2. Dissection of the fibro-fatty tissue of the Recurrent Carotid Recess with lymph node exposure (arrow).
other deep.The deep group is composed of lymph nodes distributed along the internal jugular vein (internal jugular chain).They are considered lateral lymph nodes.There are also the median lymph nodes, which are the pre-laryngeal, pre-tracheal, and the prethyroid ones.Moore and Dalley 5 describes that the drainage of the thyroid gland is initially performed to the pre-laryngeal, pre-tracheal, and paratracheal lymph nodes, and, that, in turn, drain to the and lower deep cervical lymph nodes, following towards the left thoracic ducts and right lymphatic ducts.We observed that, although all these anatomy treatises cite the paratracheal lymph nodes, the territory we detached and its respective lymph nodes (RCR) are not mentioned.Capelli 6 performed a cadaveric study quantifying the cervical lymph nodes of the lateral compartment (levels I to IV), aiming to determine a minimum number of lymph nodes in a cervical lymphadenectomy, as well as the number of lymph nodes at each level of cervical lymphadenectomy.Although we searched in Capelli's study a relationship between anthropometric and demographic data and the presence of lymph nodes found at each level, similarly to what we did in our study, we could not find the central compartment, level VI, as it was not studied.In turn, Tavares et al. 7 performed an anatomical study on cadavers, dissecting 30 central compartments to demonstrate the variability of the number of lymph nodes in this region, which ranged from two to 42.Lymph nodes specifically located lateral to the right recurrent laryngeal nerve varied in number from zero to 11, similarly to the results we found.However, their work presented no anthropometric relationship.In our study, the lymph nodes found in the RCR ranged from zero to six.Ofo et al. 8 also performed an anatomical study on cadavers, in which 28 central compartments were dissected to quantify lymph nodes in this region.The central compartment was subdivided into four regions: pre-laryngeal, right and left pretracheal, and paratracheal.The number of lymph nodes found in the compartment ranged from oneto 16, with a mean of four.In the paratracheal region, the number ranged from zero to seven, with a mean of four too.The size of the lymph nodes found throughout the compartment ranged from 0.5 to 21 mm, with a mean of 2.9mm.Here, there was also similarity to our results, since the number of lymph nodes in our study ranged from zero to six, and the mean size was of 7.82x3.86mm(longitudinal x transversal diameters).Despite the similarity of results, the work of Ofo et al.8 did not perform any correlation with anthropometric data, as what was done in our study.The existence of lymph nodes in the RCR was confirmed by this study.The number of these organs varied from zero to six in the studied specimens.Considering only those in which the lymph nodes were present, an average amount of 1.56±0.29,per cadaver, was obtained.Their size ranged from 0.9 to 5.39 mm in the transversal diameter (smaller axis), with a mean of 2.47mm, and, in the longitudinal diameter (greater axis), it ranged from 1.36 to 11.64 mm, with a mean of 5with the presence of lymph nodes in the medium-height (p=0.03) and white (p=0.04)corpses.

Table 1 .
Demographic characteristics of the study population.

Table 2 .
Relationship between anthropometric data and the presence of lymph nodes in the RCR (Fisher's exact test).

Table 3 .
Relationship between race and the presence of lymph nodes in the RCR (Fisher's exact test).