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Nerve Ultrasound As Helpful Tool in Polyneuropathies diagnostics Review Nerve Ultrasound as Helpful Tool in Polyneuropathies Magdalena Kramer 1, Alexander Grimm 1,*, Natalie Winter 1, Marc Dörner 1,2 , Kathrin Grundmann-Hauser 3, Jan-Hendrik Stahl 1, Julia Wittlinger 1, Josua Kegele 1, Cornelius Kronlage 1 and Sophia Willikens 1 1 Department of Neurology and Epileptology, Tübingen University Hospital and Hertie Institute for Clinical Brain Research, Eberhard Karls University Tübingen, 72076 Tübingen, Germany; [email protected] (M.K.); [email protected] (N.W.); [email protected] (M.D.); [email protected] (J.-H.S.); [email protected] (J.W.); [email protected] (J.K.); [email protected] (C.K.); [email protected] (S.W.) 2 Department of Forensic Psychiatry, University Hospital of Psychiatry Zurich, University of Zurich, 8008 Zurich, Switzerland 3 Institute of Medical Genetics and Applied Genomics, Tübingen University Hospital, Eberhard Karls University Tübingen, 72076 Tübingen, Germany; [email protected] * Correspondence: [email protected]; Tel.: +49-7071-29-0 Abstract: Background: Polyneuropathies (PNP) are a broad field of diseases affecting millions of people. While the symptoms presented are mostly similar, underlying causes are abundant. Thus, early identification of treatable causes is often difficult. Besides clinical data and basic laboratory find- ings, nerve conduction studies are crucial for etiological classification, yet limited. Besides Magnetic Resonance Imaging (MRI), high-resolution nerve ultrasound (HRUS) has become a noninvasive, fast, economic and available tool to help distinguish different types of nerve alterations in neuropathies. Methods: We aim to describe typical ultrasound findings in PNP and patterns of morphological changes in hereditary, immune-mediated, diabetic, metabolic and neurodegenerative PNP. Literature Citation: Kramer, M.; Grimm, A.; research was performed in PubMed using the terms ‘nerve ultrasound’, neuromuscular ultrasound, Winter, N.; Dörner, M.; high-resolution nerve ultrasound, peripheral nerves, nerve enlargement, demyelinating, hereditary, Grundmann-Hauser, K.; Stahl, J.-H.; Wittlinger, J.; Kegele, J.; Kronlage, C.; polyneuropathies, hypertrophy’. Results: Plenty of studies over the past 20 years investigated the Willikens, S. Nerve Ultrasound as value of nerve ultrasound in different neuropathies. Next to nerve enlargement, patterns of nerve Helpful Tool in Polyneuropathies. enlargement, echointensity, vascularization and elastography have been evaluated for diagnostic Diagnostics 2021, 11, 211. https:// terms. Furthermore, different scores have been developed to distinguish different etiologies of PNP. doi.org/10.3390/diagnostics11020211 Conclusions: Where morphological alterations of the nerves reflect underlying pathologies, early nerve ultrasound might enable a timely start of available treatment and also facilitate follow up of Academic Editor: Rute Santos therapy success. Received: 30 December 2020 Accepted: 27 January 2021 Keywords: high-resolution nerve ultrasound; peripheral nerve imaging; demyelinating polyneu- Published: 31 January 2021 ropathies; hereditary polyneuropathies Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- 1. Introduction iations. Polyneuropathies are among the most frequent neurological disorders and cause significant morbidity and use of resources. Finding the cause of neuropathic deficits still remains a challenge in daily clinical routine. Although technical tools have improved and nerve conduction studies, skin and nerve biopsy, next generation sequencing, cere- Copyright: © 2021 by the authors. brospinal fluid (CSF) analysis or antibody testing are established methods, the cause of Licensee MDPI, Basel, Switzerland. PNP remains unclear in up to one third of patients. Imaging tools such as MRI of the roots This article is an open access article distributed under the terms and and nerves could contribute to the diagnosis of immune-mediated neuropathies, hereditary conditions of the Creative Commons transthyretin (TTR) associated systemic amyloidosis and others in the recent past [1–3]. Attribution (CC BY) license (https:// However, their use is still limited to specialized centers. In contrast, ultrasound is a widely creativecommons.org/licenses/by/ distributed tool, which is able to visualize nerves and roots with high resolution and 4.0/). accuracy. A growing number of studies has been published in the last decade concerning Diagnostics 2021, 11, 211. https://doi.org/10.3390/diagnostics11020211 https://www.mdpi.com/journal/diagnostics Diagnostics 2021, 11, 211 2 of 23 ultrasound findings in polyneuropathies [4,5]. The aim of this review is to give an overview and to propose an algorithm for examination of patients with suspected PNP including nerve ultrasound and nerve conduction studies. 2. Ultrasound Parameters in Neuropathies Several aspects can be visualized and measured by ultrasound [6,7]. Before scanning the nerves, the examiner must be aware of the normal nerve appearance, especially in regard to nerve size, nerve and fascicle anatomy, echointensity, vascularity, elastography and surrounding tissue morphology (example is given in Figure1). For differentiation of PNP the following parameters have been proven to be most useful: (1) The most simple feature is the enlargement of cross-sectional area (CSA), which can be seen either focally restricted (one short nerve segment), regionally (larger nerve segments) or diffusely (the whole nerve) within one nerve (unifocal), several nerves (multifocal) or all nerves and roots (generalized) (Figure2). Further, nerve enlargement can exhibit certain predominance (e.g., proximal enlargement including the roots, the plexus and the proximal segments of the nerves). (2) CSA enlargement is typically more often seen in demyelinating neuropathies than in axonal types. Next to CSA enlargement of the whole nerve, some PNP reveal a fascicular enlargement pattern, in which one or more fascicles can be involved. In patients with multifocal motor neuropathy (MMN) single fascicles are enlarged next to normal sized fascicles (Figure3D) [ 8,9]. Fascicle enlargement in PNP can also be regional (some fascicles enlarged in some nerves, sparing other nerves), differential (sparing some fascicles, but affecting all nerves) or generalized (affecting all fascicles and all nerves) (3). Depending on the number and size of affected fascicles, the CSA of the whole nerve can be enlarged as well. However, fascicle visualization and thus size interpretation must be handled with caution because the resolution and therefore the probe frequency plays an important role [8,10]. Recently, the focus has been further set on nerve echointensity [11–14]. The echo signal of the healthy nerve contains the hyperechoic area (i.e., the epineurium, the perineurium) and hypoechoic area (i.e., the nerve bundles). Padua and colleagues already described echointensity changes in some patients with chronic inflammatory demyelinating polyneuropathies (CIDP) [11]. Similar findings have been made by Haertig et al. and Fisse et al. [12,13]. Taken together, next to nerve enlargement, nerves can be hyperechoic (particularly fascicles due to scar tissue, fibrosis or axonal damage) or hypoechoic (maybe provoked by inflammation or edema). The qualitative description of the echo signal might be more suitable for daily routine; however, the quantitative analysis by software tools (grey scale analysis and fraction of black) is increasingly used as a more common method. (4) Concerning nerve vascularity, nerve elastography and the perinerval tissue, new insights have been published [15,16], but its role in PNP still remains unclear and thus description of these methods will not be discussed at this point. Diagnostics 2021, 11, 211 3 of 23 Diagnostics 2021, 11, 211 3 of 22 Figure 1. Cross-sectional and longitudinal view of a normal median nerve at forearm level. (A) Cross-sectional view of Figure 1. Cross-sectionalthe median nerve. and The longitudinal nerve appearance view isof honey-comb-like a normal median with hypoechoic nerve at fascicles forearm and level. hyperechoic (A) Cross-sectional epi- and peri- view of the median nerve.neurium. The nerve (B,C) appearanceMeasurement techniques is honey-comb-like of the cross-sectional with hypoechoicarea (CSA) using fascicles the free-hand and ( hyperechoicB, upper picture) epi- or ellipse and perineurium. B C function (C, lower picture) of the ultrasound device, CSA 5 mm². (D) Longitudinal view ofB the median nerve in pano- ( , ) Measurementramic view. techniques Left side of of the the picture: cross-sectional entrance into carpal area (CSA)tunnel. Arrow using heads the free-handare marking the ( , nerve, upper asterisks picture) the super- or ellipse function (C, lower picture)ficial and of theflexor ultrasound digitorum muscles, device, the CSAcircle 5the mm radial2.( arteryD) Longitudinal and the x the radial view bone, of “A” the in median pictures nerveB and C in means panoramic view. Left side of the“area” picture:. entrance into carpal tunnel. Arrow heads are marking the nerve, asterisks the superficial and flexor Diagnostics 2021, 11, 211 4 of 22 digitorum muscles, the circle the radial artery and the x the radial bone, “A” in pictures B and C means “area”. Figure 2. ExamplesFigure 2. ofExamples altered of nervealtered
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