Abstract
The aim of this article is to utilize ultrasound to evaluate the normal cross-sectional area (CSA)of the vagus nerve (VN) in the carotid sheath. This study included 86 VNs in 43 healthy subjects (15 men, 28 women); mean age 42.1 years and mean body mass index 26.2 kg/m2. For each subject, the bilateral VNs were identified by US at the anterolateral neck within the common carotid sheaths. One radiologist obtained 3 separate CSA measurements for each of the bilateral VNs with complete transducer removal between each measurement. Additionally, for each participant, demographic information of age and gender as well as body mass index, weight, and height were documented. The mean CSA of the right VN in the carotid sheath was 2.1 and 1.9 mm2 for the left VN. The right VN CSA was significantly larger than the left VN (P < .012). No statistically significant correlation was noted in relation to height, weight, and age. We believe that the reference values for the normal CSA of the VN obtained in our study, could help in the sonographic evaluation of VN enlargement, as it relates to the diagnosis of various diseases affecting the VN.
Keywords: carotid sheath, cross-sectional area, reference values, sonographic, ultrasound, Vagus nerve
1. Introduction
The vagus nerve (VN) is the longest cranial nerve (cranial nerve X) which arises from the brainstem, exiting the medulla below the ninth cranial nerve, and extending through the jugular foramen. It descends in the neck, residing inside the carotid sheath, posteromedial to the internal jugular vein and posterolateral to the common carotid artery.[1–4] The VN fascicles serve a parasympathetic function in swallowing and phonation as well as autonomic regulation.[5,6] The superior branches of the VN innervate the muscles of the larynx, pharynx, and palate. They also supply lower cervical and thoraco-abdominal parasympathetic fibers. Sensory fibers are supplied to the gastrointestinal and respiratory visceral mucosa. The VN contributes in the involuntary control of the cardiac and smooth muscles in addition to the secretory part of the intestine. Voluntary motor control is provided to the anterior cervical skeletal muscles.[7]
Knowledge of the normal cross sectional area (CSA) of the VN would be expected to offer insight in regard to abnormalities of the VN as well as diseases affecting the VN, and potentially subsequent dysregulation of the autonomic nervous system.[8] As nerve ultrasound emerges as an important diagnostic tool, multiple studies have begun providing normal CSA reference values of multiple nerves to assist in the diagnosis of related neuropathies. Additionally, utilization of ultrasound of the VN has been documented for the use in various diseases including diabetes mellitus, Parkinson’s disease, multifocal motor neuropathy, chronic inflammatory demyelinating polyradiculoneuropathy, amyotrophic lateral sclerosis, Charcot–Marie-Tooth disease, systemic vasculitic neuropathy, and atrial fibrillation.[9–24] Moreover, VN stimulation for the management of epilepsy has gained popularity in the last few years.[25] Furthermore, VN stimulation has been documented for the management of intractable hiccoughs (hiccups).[26] Additional uses for VN ultrasound include intraoperative neuromonitoring of thyroid surgery, radiofrequency ablation of thyroid nodules, and assessment of vocal cord paralysis.[27–29] However, there is significant variation in the currently published VN CSAs in the normal healthy population.[30] Therefore, the aim of this study is to use ultrasound to evaluate the normal VN CSA in the carotid sheath.
2. Methods
2.1. Participants
This study was performed in accordance with the ethical standards of our institutional research committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards. Institutional review board approval was obtained for this prospective study, and written, informed consent was obtained. Our study complied with the Health Insurance Portability and Accountability Act. Subjects participating in the study were recruited between October 2020 and October 2021. Exclusion criteria included patients with any neurological diseases or any clinical symptoms related to the nervous system. Additionally, patients with type 1 or type 2 diabetes mellitus as well as any prior neck surgery were excluded from the study. For each participant, demographic information of age and gender as well as body mass index (BMI), weight, and height were documented.
2.2. Technique
All VN ultrasound studies were performed utilizing a L12-5-MHz linear transducer (Epic 7 version1.5, Ultrasound system; Philips, Bothell, WA). A single radiologist (M.A.B.), with greater than 10 years of experience in neuromuscular ultrasound, performed all examinations and CSA tracings. In order to identify and image the VN, all subjects were placed in a supine position with the neck in extension. The ultrasound transducer was positioned anterolaterally on the neck to identify the common carotid artery, lateral to the thyroid lobe. The VN was scanned bilaterally and identified between the common carotid artery and the internal jugular vein as a round hypoechoic fascicular structure with a normal “honeycomb” appearance (Fig. 1A). The CSA of the VN was obtained using the trace method, measuring along the inner aspect of the hyperechoic epineurium (Fig. 1B). Each subject was scanned 3 times with complete transducer removal between each CSA measurement. This resulted in 9 CSA measurements per patient.
Figure 1.
Short-axis (transverse) ultrasound images of the left vagus nerve (A) in relation to the left CCA, the SCM, the IJV, and the left thyroid lobe with (B) measurement by the tracer method. CCA = internal jugular vein, IJV = internal jugular vein, SCM = sternocleidomastoid muscle.
2.3. Statistical analysis
Statistical analysis was performed using Statistical Package for the Social Sciences (SPSS) version 21 software (SPSS Inc., Chicago, IL). Data were presented as mean ± standard deviation (SD) and range. Paired sample t-test was used to assess the differences between CSA of the right and left VNs. The associations between the mean CSA and age, weight, height, and BMI were calculated by Pearson correlation coefficient test. Statistical significance was defined as a P < .05.
3. Results
Our study included 86 VNs in 43 healthy subjects (15 men (34.9%), 28 females (65.1%)), with mean age 42.1 ± 10.7 (range: 26–66 years), mean height 161.2 ± 9.1 cm (range: 148–186), mean weight 69.7 ± 18.7 kg (range: 43–122), mean BMI 26.2 ± 5.1 kg/m2 (range 16.5–39.8). The mean CSA of the right VN was 2.1 mm2 (range 1.0–3.8 ± 0.5 SD) and of the left VN was 1.9 mm2 (range 0.9–4.0 ± 0.6 SD). The descriptive statistics of the VN are show in Table 1. The associations between age, weight, BMI, and height, with the CSA reference values of the VN are shown in Table 2. The right VN CSA was significantly larger than the left VN (P < .012). No statistically significant correlation was noted in relation to height, weight, BMI and age.
Table 1.
Showed the descriptive statistics the mean CSA values of the vagus nerve.
Mean ± SD | No | % | |
---|---|---|---|
Age in year | 42.1 ± 10.7 | ||
Gender | |||
Male | 15 | 34.9 | |
Female | 28 | 65.1 | |
Height (cm) | 161.2 ± 9.1 | ||
Weight (kg) | 69.7 ± 18.7 | ||
Body mass index | 26.2 ± 5.1 | ||
CSA right side | 2.1 ± 0.5 | P = .012 | |
CSA left side | 1.9 ± 0.6 |
CSA = cross sectional area.
Table 2.
Showed correlations between age, weight, BMI, and height, with the CSA reference values of the vagus nerve.
AGE | Weight in kg | Height in cm | BMI | ||
---|---|---|---|---|---|
CSA right side | Pearson correlation | −0.144 | −0.178 | 0.042 | −0.271 |
Sig. (2-tailed) | 0.358 | 0.254 | 0.787 | 0.079 | |
N | 43 | 43 | 43 | 43 | |
CSA left side | Pearson correlation | −0.205 | −0.251 | 0.054 | −0.315* |
Sig. (2-tailed) | 0.187 | 0.105 | 0.731 | 0.040 | |
N | 43 | 43 | 43 | 43 |
BMI = body mass index, CSA = cross sectional area.
Correlation is significant at the 0.05 level (2-tailed).
4. Discussion
We evaluated the normal CSA of the VN at the neck, within the carotid sheath, between the common carotid artery and the internal jugular vein utilizing ultrasound. The results obtained in our study (right VN = 2.1 ± 0.5 mm2, left VN = 1.9 ± 0.6 mm2), where comparable to several studies in the literature. For example, Holzapfel et al (right VN = 2.2 ± 0.6 mm2, left VN = 2.0 ± 0.3 mm2), Pelz et al (right VN = 2.6 ± 0.6 mm2, left VN = 1.9 ± 0.4 mm2), and Grimm et al (2.2 ± 0.7 mm2), demonstrated values very near to our results.[30–32] Fisse et al[8] calculated the mean pooled CSA of the VN inside the carotid sheath in 4 studies to be (2.2 mm2) which also coincides with our study. Fedtke et al[33] (right VN = 2.7 ± 0.7 mm2, left VN = 2.4 ± 0.7 mm2) and Crucean et al[34] (right VN = 2.4 ± 0.08 mm2, left VN = 2.1 ± 0.06 mm2) reported slightly higher values. Walter et al[35] (right VN = 1.32 ± 0.51 mm2, left VN = 1.12 ± 0.53 mm2) published slightly lower values compared to our study. Two studies reported exceptionally higher values; Tawfik et al (right VN = 5.8 ± 10.3 mm2, left VN = 5.5 ± 1.6 mm2) and Cartwright et al (5 ± 2 mm2).[7,9,36] The differences in CSA values between studies could be attributed to several factors including differing study cohorts, different methods of CSA measurements, different BMIs, and CSA measurements performed at different anatomic levels. Other influencing factors include the use of different ultrasound systems and the presence of motion artifact due to proximity of the pulsating vasculature.[22,30] The CSA of the VN in our study was larger on the right side compared to the left side coinciding with Pelz et al[30] and Crucean et al[34] One possible explanation is the asymmetric innervation between both sides where the right VN terminates in both the celiac plexus and the anterior gastric plexus, while the left VN terminates at the anterior gastric plexus only. This relates to the right VN additionally supplying the colon and small intestine.[37] Similar to other studies, our study demonstrated no significant correlation between the VN CSA and the demographic data.[9,30,35]
The limitations of this study should be acknowledged when interpreting the results. First, the relatively small sample size. However, although the sample size was small, scanning bilaterally allowed us to have multiple CSAs to compare. Second, all sonographic examinations were performed by a single examiner, although, the single examiner did measure 3 separate times and use the mean, a future study could be performed incorporating multiple examiners. Third, the mean age in our study was 42.1 ± 10.7 which limits generalization over the population. Further studies with a larger sample size, including more than 1 examiner, and involving different pathologies are suggested.
In conclusion, we believe that the reference values for the normal VN CSAs obtained in our study could help in the identification of various diseases where ultrasound of the VN ultrasound plays a diagnostic role. Furthermore, this study also emphasizes the importance of evaluating the VN bilaterally, given the differing side-to-side CSAs.
Acknowledgments
The authors thank the Deanship of Scientific Research at Prince Sattam Bin Abdulaziz University.
Author contributions
Conceptualization: Mohamed Abdelmohsen Bedewi, Mamdouh Ali Kotb, Daifallah Mohammed Almalki, Ali Abdullah AlAseeri.
Data curation: Mohamed Abdelmohsen Bedewi.
Formal analysis: Mohamed Abdelmohsen Bedewi.
Investigation: Mohamed Abdelmohsen Bedewi.
Methodology: Mohamed Abdelmohsen Bedewi, Mamdouh Ali Kotb, Ali Abdullah AlAseeri.
Project administration: Mohamed Abdelmohsen Bedewi.
Resources: Mohamed Abdelmohsen Bedewi, Daifallah Mohammed Almalki, Nasser M. Aldossary.
Software: Mohamed Abdelmohsen Bedewi.
Supervision: Mohamed Abdelmohsen Bedewi, Kholoud J. Sandougah, Bader A. Alhariqi, Tariq Alfaifi.
Validation: Mohamed Abdelmohsen Bedewi.
Visualization: Mohamed Abdelmohsen Bedewi.
Writing – original draft: Mohamed Abdelmohsen Bedewi.
Writing – review & editing: Mohamed Abdelmohsen Bedewi, Ramy Abdelnaby, Steven B. Soliman.
Abbreviations:
- BMI
- Body mass index
- CSA
- Cross sectional area
- SD
- standard deviation
- VN
- Vagus nerve
The authors have no funding and conflicts of interest to disclose.
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
How to cite this article: Bedewi MA, Kotb MA, Almalki DM, AlAseeri AA, Sandougah KJ, Abdelnaby R, Soliman SB, Alhariqi BA, Alfaifi T, Aldossary NM. Ultrasound of the normal vagus nerve cross-sectional area in the carotid sheath. Medicine 2023;102:23(e33996).
Contributor Information
Mamdouh Ali Kotb, Email: alikotb1970@gmail.com.
Daifallah Mohammed Almalki, Email: dr_daifullah@hotmail.com.
Ali Abdullah AlAseeri, Email: dralialaseeri@gmail.com.
Kholoud J. Sandougah, Email: Ksandougah@imamu.edu.sa.
Ramy Abdelnaby, Email: Rabdelnaby@ukaachen.de.
Steven B. Soliman, Email: ssoliman@med.umich.edu.
Bader A. Alhariqi, Email: dr.bader25@gmail.com.
Tariq Alfaifi, Email: dr.tmf87@gmail.com.
Nasser M. Aldossary, Email: draldossary@hotmail.com.
References
- [1].Baquiran M, Bordoni B. Anatomy, Head and Neck, Anterior Vagus Nerve. Treasure Island, FL: StatPearls Publishing; 2022. [PubMed] [Google Scholar]
- [2].Chen HH, Chen TC, Yang TL, et al. Transcutaneous sonography for detection of the cervical vagus nerve. Ear Nose Throat J. 2021;100:155–9. [DOI] [PubMed] [Google Scholar]
- [3].Giovagnorio F, Martinoli C. Sonography of the cervical vagus nerve: normal appearance and abnormal findings. AJR Am J Roentgenol. 2001;176:745–9. [DOI] [PubMed] [Google Scholar]
- [4].Ottaviani MM, Wright L, Dawood T, et al. In vivo recordings from the human vagus nerve using ultrasound-guided microneurography. J Physiol. 2020;598:3569–76. [DOI] [PubMed] [Google Scholar]
- [5].Browning KN, Verheijden S, Boeckxstaens GE. The Vagus nerve in appetite regulation, mood, and intestinal inflammation. Gastroenterology. 2017;152:730–44. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [6].Ahmed U, Chang YC, Zafeiropoulos S, et al. Strategies for precision vagus neuromodulation. Bioelectron Med. 2022;8:9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [7].Tawfik EA, Walker FO, Cartwright MS. Neuromuscular ultrasound of cranial nerves. J Clin Neurol. 2015;11:109–21. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [8].Fisse AL, Katsanos AH, Gold R, et al. Cross-sectional area reference values for peripheral nerve ultrasound in adults: a systematic review and meta-analysis-Part III: cervical nerve roots and vagal nerve. Eur J Neurol. 2021;28:2319–26. [DOI] [PubMed] [Google Scholar]
- [9].Tawfik EA, Walker FO, Cartwright MS, et al. Diagnostic ultrasound of the vagus nerve in patients with diabetes. J Neuroimaging. 2017;27:589–93. [DOI] [PubMed] [Google Scholar]
- [10].Sijben LCJ, Mess WH, Walter U, et al. The cross-sectional area of the vagus nerve is not reduced in Parkinson’s disease patients. eNeurologicalSci. 2022;27:100400. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [11].Tsukita K, Taguchi T, Sakamaki-Tsukita H, et al. The vagus nerve becomes smaller in patients with Parkinson’s disease: a preliminary cross-sectional study using ultrasonography. Parkinsonism Relat Disord. 2018;55:148–9. [DOI] [PubMed] [Google Scholar]
- [12].Abdelnaby R, Elsayed M, Mohamed KA, et al. Vagus nerve ultrasonography in Parkinson’s disease: a systematic review and meta-analysis. Auton Neurosci. 2021;234:102835. [DOI] [PubMed] [Google Scholar]
- [13].Rattay TW, Winter N, Decard BF, et al. Nerve ultrasound as follow-up tool in treated multifocal motor neuropathy. Eur J Neurol. 2017;24:1125–34. [DOI] [PubMed] [Google Scholar]
- [14].Niu J, Zhang L, Ding Q, et al. Vagus nerve ultrasound in chronic inflammatory demyelinating polyradiculoneuropathy and charcot-marie-tooth disease type 1A. J Neuroimaging. 2020;30:910–6. [DOI] [PubMed] [Google Scholar]
- [15].Cartwright MS, Brown ME, Eulitt P, et al. Diagnostic nerve ultrasound in Charcot-Marie-Tooth disease type 1B. Muscle Nerve. 2009;40:98–102. [DOI] [PubMed] [Google Scholar]
- [16].Pelz JO, Belau E, Fricke C, et al. Axonal degeneration of the Vagus nerve in Parkinson’s disease – a high-resolution ultrasound study. Front Neurol. 2018;9:951. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [17].Tawfik EA. Vagus nerve ultrasound in a patient with amyotrophic lateral sclerosis. Muscle Nerve. 2016;54:978–9. [DOI] [PubMed] [Google Scholar]
- [18].Grimm A, Decard BF, Bischof A, et al. Ultrasound of the peripheral nerves in systemic vasculitic neuropathies. J Neurol Sci. 2014;347:44–9. [DOI] [PubMed] [Google Scholar]
- [19].Grimm A, Decard BF, Athanasopoulou I, et al. Nerve ultrasound for differentiation between amyotrophic lateral sclerosis and multifocal motor neuropathy. J Neurol. 2015;262:870–80. [DOI] [PubMed] [Google Scholar]
- [20].Jang JH, Cho CS, Yang KS, et al. Pattern analysis of nerve enlargement using ultrasonography in chronic inflammatory demyelinating polyneuropathy. Clin Neurophysiol. 2014;125:1893–9. [DOI] [PubMed] [Google Scholar]
- [21].Grimm A, Rasenack M, Athanasopoulou I, et al. Long-term observations in asymmetric immune-mediated neuropathy with vagus hypertrophy using ultrasound of the nerves. J Neurol Sci. 2015;356:205–8. [DOI] [PubMed] [Google Scholar]
- [22].Holzapfel K, Naumann M. Ultrasound detection of vagus nerve atrophy in bulbar amyotrophic lateral sclerosis. J Neuroimaging. 2020;30:762–5. [DOI] [PubMed] [Google Scholar]
- [23].Du K, Xu K, Chu X, et al. Vagus nerve ultrasound in transthyretin familial amyloid polyneuropathy: a pilot study. J Neuroimaging. 2022;32:285–91. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [24].Oura K, Itabashi R, Yamaguchi Oura M, et al. Cross-sectional area of the vagus nerve on carotid duplex ultrasound and atrial fibrillation in acute stroke: a retrospective analysis. eNeurologicalSci. 2021;25:100378. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [25].Verlinden TJ, Rijkers K, Hoogland G, et al. Morphology of the human cervical vagus nerve: implications for vagus nerve stimulation treatment. Acta Neurol Scand. 2016;133:173–82. [DOI] [PubMed] [Google Scholar]
- [26].Gong WY, Li N, Chen J, et al. Treatment of intractable hiccups using combined cervical vagus nerve and phrenic nerve blocks under ultrasound guidance. Minerva Anestesiol. 2021;87:1050–1. [DOI] [PubMed] [Google Scholar]
- [27].Hartl DM, Bidault S, Girard E, et al. Ultrasound visualization of the vagus nerve for intraoperative neuromonitoring in thyroid surgery. Eur Radiol. 2021;31:4063–70. [DOI] [PubMed] [Google Scholar]
- [28].Wang CP, Chen TC, Lou PJ, et al. Neck ultrasonography for the evaluation of the etiology of adult unilateral vocal fold paralysis. Head Neck. 2012;34:643–8. [DOI] [PubMed] [Google Scholar]
- [29].Ha EJ, Baek JH, Lee JH, et al. Clinical significance of vagus nerve variation in radiofrequency ablation of thyroid nodules. Eur Radiol. 2011;21:2151–7. [DOI] [PubMed] [Google Scholar]
- [30].Pelz JO, Belau E, Henn P, et al. Weise D Sonographic evaluation of the vagus nerves: protocol, reference values, and side-to-side differences. Muscle Nerve. 2018;57:766–71. [DOI] [PubMed] [Google Scholar]
- [31].Grimm A, Decard BF, Schramm A, et al. Ultrasound and electrophysiologic findings in patients with Guillain-Barre syndrome at disease onset and over a period of six months. Clin Neurophysiol. 2016;127:1657–63. [DOI] [PubMed] [Google Scholar]
- [32].Grimm A, Decard BF, Axer H. Ultrasonography of the peripheral nervous system in the early stage of Guillain-Barre syndrome. J Peripher Nerv Syst. 2014;19:234–41. [DOI] [PubMed] [Google Scholar]
- [33].Fedtke N, Witte OW, Prell T. Ultrasonography of the vagus nerve in Parkinson’s disease. Front Neurol. 2018;9:525. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [34].Curcean AD, Rusu GM, Dudea SM. Ultrasound appearance of peripheral nerves in the neck: vagus, hypoglossal and greater auricular. Med Pharm Rep. 2020;93:39–46. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [35].Walter U, Tsiberidou P, Kersten M, et al. Atrophy of the vagus nerve in Parkinson’s disease revealed by high-resolution ultrasonography. Front Neurol. 2018;9:805. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [36].Cartwright MS, Passmore LV, Yoon JS, et al. Cross-sectional area reference values for nerve ultrasonography. Muscle Nerve. 2008;37:566–71. [DOI] [PubMed] [Google Scholar]
- [37].Drakonaki E, Clouverakis G, Piagkou M, et al. Normal anatomy, variants and factors associated with the cervical vagus nerve topography: a high-resolution ultrasound study. Surg Radiol Anat. 2021;43:1753–64. [DOI] [PubMed] [Google Scholar]