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Ultrasound characteristics of the cervical vagus nerve in patients with type 2 diabetes and diabetic peripheral neuropathy
- Department of Endocrinology, The Affiliated Wuxi People’s Hospital of Nanjing Medical University, Wuxi People’s Hospital, Wuxi Medical Centre, Nanjing Medical University, Wuxi, China
- Department of Geriatrics, Nanjing Drum Tower Hospital, the Affiliated Hospital of Nanjing University Medical School, Nanjing, China
- Department of Ultrasound, The Affiliated Wuxi People’s Hospital of Nanjing Medical University, Wuxi People’s Hospital, Wuxi Medical Centre, Nanjing Medical University, Wuxi, China
open access
Abstract
Introduction: Diabetic peripheral neuropathy (DPN) and autonomic neuropathy are commonly coexistent in patients with type 2 diabetes mellitus (T2DM). Current assessment tools for diabetic neuropathy remain complicated and limited. We aimed to investigate the sonographic changes of the cervical vagus nerve in DPN patients with T2DM.
Material and methods: Patients with T2DM were divided into a DPN group (DPN, n = 44) and non-DPN controls (NDPN, n = 43) based on electromyogram results. Another 43 healthy controls (CON) were included. High-frequency ultrasound (HFU) of the vagus nerve was performed in all participants.
Results: Compared with controls, the honeycomb structure of the vagus nerve in patients with T2DM decreased, p < 0.001. The DPN group had higher cross-sectional area (CSA) of the right vagus nerve than the NDPN group (1.60 ± 0.52 vs. 2.00 ± 0.57 mm2, p =0.001). Logistic regression showed that right vagus nerve CSA was a risk factor of DPN (odds ratio [OR] = 3.924, p = 0.002). Right vagus nerve CSA was positively correlated with diabetes duration (p = 0.003), and negatively correlated with the motor conduction velocity (MCV) of the ulnar, median, and common peroneal nerves (p < 0.001 for all), as well as the sensor conduction velocity (SCV) of the ulnar and median nerve (both p < 0.005).
Conclusion: HFU shows thickening of the cervical vagus nerve in patients with DPN, which is a potential diagnostic feature of diabetic neuropathy.
Abstract
Introduction: Diabetic peripheral neuropathy (DPN) and autonomic neuropathy are commonly coexistent in patients with type 2 diabetes mellitus (T2DM). Current assessment tools for diabetic neuropathy remain complicated and limited. We aimed to investigate the sonographic changes of the cervical vagus nerve in DPN patients with T2DM.
Material and methods: Patients with T2DM were divided into a DPN group (DPN, n = 44) and non-DPN controls (NDPN, n = 43) based on electromyogram results. Another 43 healthy controls (CON) were included. High-frequency ultrasound (HFU) of the vagus nerve was performed in all participants.
Results: Compared with controls, the honeycomb structure of the vagus nerve in patients with T2DM decreased, p < 0.001. The DPN group had higher cross-sectional area (CSA) of the right vagus nerve than the NDPN group (1.60 ± 0.52 vs. 2.00 ± 0.57 mm2, p =0.001). Logistic regression showed that right vagus nerve CSA was a risk factor of DPN (odds ratio [OR] = 3.924, p = 0.002). Right vagus nerve CSA was positively correlated with diabetes duration (p = 0.003), and negatively correlated with the motor conduction velocity (MCV) of the ulnar, median, and common peroneal nerves (p < 0.001 for all), as well as the sensor conduction velocity (SCV) of the ulnar and median nerve (both p < 0.005).
Conclusion: HFU shows thickening of the cervical vagus nerve in patients with DPN, which is a potential diagnostic feature of diabetic neuropathy.
Keywords
high-frequency ultrasound; vagus nerve cross-sectional area; diabetic peripheral neuropathy
Title
Ultrasound characteristics of the cervical vagus nerve in patients with type 2 diabetes and diabetic peripheral neuropathy
Journal
Issue
Article type
Original paper
Pages
421-429
Published online
2023-08-08
Page views
964
Article views/downloads
347
DOI
Pubmed
Bibliographic record
Endokrynol Pol 2023;74(4):421-429.
Keywords
high-frequency ultrasound
vagus nerve cross-sectional area
diabetic peripheral neuropathy
Authors
Fan Xiong
Qian Wang
Yun Hu
Xiao Jiang
Lin Liu
Yumeng Han
Qing Jiang
Shiqin Yuan
Lan Xu
- Sun H, Saeedi P, Karuranga S, et al. IDF Diabetes Atlas: Global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res Clin Pract. 2022; 183: 109119.
- Didangelos T, Veves A. Treatment of Diabetic Cardiovascular Autonomic, Peripheral and Painful Neuropathy. Focus on the Treatment of Cardiovascular Autonomic Neuropathy with ACE Inhibitors. Curr Vasc Pharmacol. 2020; 18(2): 158–171.
- Vinik AI, Nevoret ML, Casellini C, et al. Diabetic neuropathy. Endocrinol Metab Clin North Am. 2013; 42(4): 747–787.
- Vinik AI, Casellini C, Névoret ML. Alternative Quantitative Tools in the Assessment of Diabetic Peripheral and Autonomic Neuropathy. Int Rev Neurobiol. 2016; 127: 235–285.
- Zhao Z, Ji L, Zheng L, et al. Effectiveness of clinical alternatives to nerve conduction studies for screening for diabetic distal symmetrical polyneuropathy: A multi-center study. Diabetes Res Clin Pract. 2016; 115: 150–156.
- Pop-Busui R, Boulton AJM, Feldman EL, et al. Diabetic Neuropathy: A Position Statement by the American Diabetes Association. Diabetes Care. 2017; 40(1): 136–154.
- Narayan S, Goel A, Singh AK, et al. High resolution ultrasonography of peripheral nerves in diabetic patients to evaluate nerve cross sectional area with clinical profile. Br J Radiol. 2021; 94(1121): 20200173.
- Ma X, Li T, Du L, et al. Applicability of High-Frequency Ultrasound to the Early Diagnosis of Diabetic Peripheral Neuropathy. Biomed Res Int. 2021; 2021: 5529063.
- Ishibashi F, Taniguchi M, Kojima R, et al. Morphological changes of the peripheral nerves evaluated by high-resolution ultrasonography are associated with the severity of diabetic neuropathy, but not corneal nerve fiber pathology in patients with type 2 diabetes. J Diabetes Investig. 2015; 6(3): 334–342.
- Chen HH, Chen TC, Yang TL, et al. Transcutaneous Sonography for Detection of the Cervical Vagus Nerve. Ear Nose Throat J. 2021; 100(3): 155–159.
- Tawfik EA, Walker FO, Cartwright MS, et al. Diagnostic Ultrasound of the Vagus Nerve in Patients with Diabetes. J Neuroimaging. 2017; 27(6): 589–593.
- Haq T, Ahmed T, Latif ZA, et al. Cardiac autonomic neuropathy in patients with type 2 diabetes mellitus having peripheral neuropathy: A cross-sectional study. Diabetes Metab Syndr. 2019; 13(2): 1523–1528.
- Dyck PJ, Albers JW, Andersen H, et al. Toronto Expert Panel on Diabetic Neuropathy. Diabetic polyneuropathies: update on research definition, diagnostic criteria and estimation of severity. Diabetes Metab Res Rev. 2011; 27(7): 620–628.
- Braffett BH, Gubitosi-Klug RA, Albers JW, et al. DCCT/EDIC Research Group. Risk Factors for Diabetic Peripheral Neuropathy and Cardiovascular Autonomic Neuropathy in the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications (DCCT/EDIC) Study. Diabetes. 2020; 69(5): 1000–1010.
- Shabeeb D, Najafi M, Hasanzadeh G, et al. Electrophysiological measurements of diabetic peripheral neuropathy: A systematic review. Diabetes Metab Syndr. 2018; 12(4): 591–600.
- Funakoshi S, Fujimoto S, Hamasaki A, et al. Utility of indices using C-peptide levels for indication of insulin therapy to achieve good glycemic control in Japanese patients with type 2 diabetes. J Diabetes Investig. 2011; 2(4): 297–303.
- Zilliox L, Peltier AC, Wren PA, et al. Assessing autonomic dysfunction in early diabetic neuropathy: the Survey of Autonomic Symptoms. Neurology. 2011; 76(12): 1099–1105.
- Sletten DM, Suarez GA, Low PA, et al. COMPASS 31: a refined and abbreviated Composite Autonomic Symptom Score. Mayo Clin Proc. 2012; 87(12): 1196–1201.
- Curcean AD, Rusu GM, Dudea SM. Ultrasound appearance of peripheral nerves in the neck: vagus, hypoglossal and greater auricular. Med Pharm Rep. 2020; 93(1): 39–46.
- Abdelnaby R, Elsayed M, Mohamed KA, et al. Sonographic Reference Values of Vagus Nerve: A Systematic Review and Meta-analysis. J Clin Neurophysiol. 2022; 39(1): 59–71.
- Huang H, Wu S. Application of High-Resolution Ultrasound on Diagnosing Diabetic Peripheral Neuropathy. Diabetes Metab Syndr Obes. 2021; 14: 139–152.
- Jack M, Wright D. Role of advanced glycation endproducts and glyoxalase I in diabetic peripheral sensory neuropathy. Transl Res. 2012; 159(5): 355–365.
- Pelz JO, Belau E, Henn P, et al. Sonographic evaluation of the vagus nerves: Protocol, reference values, and side-to-side differences. Muscle Nerve. 2018; 57(5): 766–771.
- Singh KP, Gupta K, Kataria N, et al. High-resolution ultrasonography of the sural nerve in diabetic peripheral neuropathy. J Ultrason. 2020; 20(81): e83–e89.
- Singh K, Gupta K, Kaur S. High resolution ultrasonography of the tibial nerve in diabetic peripheral neuropathy. J Ultrason. 2017; 17(71): 246–252.
- Kang S, Kim SeH, Yang SN, et al. Sonographic features of peripheral nerves at multiple sites in patients with diabetic polyneuropathy. J Diabetes Complications. 2016; 30(3): 518–523.
- Lee D, Dauphinée DM. Morphological and functional changes in the diabetic peripheral nerve: using diagnostic ultrasound and neurosensory testing to select candidates for nerve decompression. J Am Podiatr Med Assoc. 2005; 95(5): 433–437.
- Zaharia OP, Strassburger K, Strom A, et al. German Diabetes Study Group. Risk of diabetes-associated diseases in subgroups of patients with recent-onset diabetes: a 5-year follow-up study. Lancet Diabetes Endocrinol. 2019; 7(9): 684–694.
- Akaza M, Akaza I, Kanouchi T, et al. Nerve conduction study of the association between glycemic variability and diabetes neuropathy. Diabetol Metab Syndr. 2018; 10: 69.
- Mohseni S. Hypoglycemic neuropathy. Acta Neuropathol. 2001; 102(5): 413–421.
- Makhmutova M, Weitz J, Tamayo A, et al. Pancreatic β-Cells Communicate With Vagal Sensory Neurons. Gastroenterology. 2021; 160(3): 875–888.e11.
- Charpentier J, Waget A, Klopp P, et al. Lixisenatide requires a functional gut-vagus nerve-brain axis to trigger insulin secretion in controls and type 2 diabetic mice. Am J Physiol Gastrointest Liver Physiol. 2018; 315(5): G671–G684.
- Al-Kureischi K. Verlauf und Nervenfaserarten des Truncus vagalis des Menschen . Acta Anat (Basel). 1979; 103(3): 252–258.
- Holzapfel K, Naumann M. Ultrasound Detection of Vagus Nerve Atrophy in Bulbar Amyotrophic Lateral Sclerosis. J Neuroimaging. 2020; 30(6): 762–765.
- Pelz JO, Belau E, Menze I, et al. Correlation between sonographic morphology and function of the cervical vagus nerves. Auton Neurosci. 2019; 220: 102552.
- Sartucci F, Bocci T, Santin M, et al. High-resolution ultrasound changes of the vagus nerve in idiopathic Parkinson's disease (IPD): a possible additional index of disease. Neurol Sci. 2021; 42(12): 5205–5211.
- 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.