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Identification of Sensory and Motor Nerve Fascicles By Zhou et al. J Transl Med (2021) 19:207 https://doi.org/10.1186/s12967-021-02871-w Journal of Translational Medicine RESEARCH Open Access Identifcation of sensory and motor nerve fascicles by immunofuorescence staining after peripheral nerve injury Xijie Zhou1,2, Jian Du2, Liming Qing2, Thomas Mee2, Xiang Xu2, Zhuoran Wang2, Cynthia Xu2 and Xiaofeng Jia2,3,4,5,6* Abstract Background: Inappropriate matching of motor and sensory fbers after nerve repair or nerve grafting can lead to fail- ure of nerve recovery. Identifcation of motor and sensory fbers is important for the development of new approaches that facilitate neural regeneration and the next generation of nerve signal-controlled neuro-prosthetic limbs with sen- sory feedback technology. Only a few methods have been reported to diferentiate sensory and motor nerve fascicles, and the reliability of these techniques is unknown. Immunofuorescence staining is one of the most commonly used methods to distinguish sensory and motor nerve fbers, however, its accuracy remains unknown. Methods: In this study, we aim to determine the efcacy of popular immunofuorescence markers for motor and sensory nerve fbers. We harvested the facial (primarily motor fascicles) and sural (primarily sensory fascicles) nerves in rats, and examined the immunofuorescent staining expressions of motor markers (choline acetyltransferase (ChAT), tyrosine kinase (TrkA)), and sensory markers [neuroflament protein 200 kDa (NF-200), calcitonin gene-related peptide (CGRP) and Transient receptor potential vanillic acid subtype 1 (TRPV1)]. Three methods, including the average area percentage, the mean gray value, and the axon count, were used to quantify the positive expression of nerve markers in the immunofuorescence images. Results: Our results suggest the mean gray value method is the most reliable method. The mean gray value of immunofuorescence in ChAT (63.0 0.76%) and TRKA (47.6 0.43%) on the motor fascicles was signifcantly higher than that on the sensory fascicles (ChAT:± 49.2 0.72%, P < 0.001;± and TRKA: 29.1 0.85%, P < 0.001). Additionally, the mean gray values of TRPV1 (51.5 0.83%), NF-200± (61.5 0.62%) and CGRP (37.7± 1.22%) on the motor fascicles were signifcantly lower than that± on the sensory fascicles± respectively (71.9 2.32%,± 69.3 0.46%, and 54.3 1.04%) (P < 0.001). The most accurate cutpoint occurred using CHAT/CRCP ratio, where± a value of ±0.855 had 100% sensitivity± and 100% specifcity to identify motor and sensory nerve with an area under the ROC curve of 1.000 (P < 0.001). Conclusions: A combination of ChAT and CGRP is suggested to distinguish motor and sensory nerve fbers. Keywords: Peripheral nerve, Immunofuorescence staining, Motor fascicles, Sensory fascicles Background Peripheral nerve injury can lead to the loss of motor, sen- *Correspondence: [email protected] sory and autonomic nerve function in the body’s gan- 2 Department of Neurosurgery, University of Maryland School glion segment, which seriously afects patients’ quality of Medicine, 10 South Pine Street, MSTF Building 823, Baltimore, MD of life [1]. Mismatched nerve fascicle repair after periph- 21201, USA Full list of author information is available at the end of the article eral nerve injury may result in partial or complete loss © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Zhou et al. J Transl Med (2021) 19:207 Page 2 of 12 of function [2]. Despite several decades of progress in immunohistochemistry, immunofuorescence can carry research and surgical techniques, surgeons still rely on out a reaction with multiple markers. Antibody-coupled experience to estimate the characteristics of damaged fuorescence can also increase the resolution [16]. motor or sensory nerve stumps and perform a diferen- Although immunofuorescence is widely used, the ef- tiated fascicular repair. Tus, a satisfactory recovery is cacy/accuracy of popular immunofuorescence mark- often difcult to achieve [3]. We have shown a 3-dimen- ers for motor and sensory nerve fbers remains unclear. sional, printed scafold repair technology promoting In addition, the results of quantitative processing meth- neural regeneration with bifurcating sensory and motor ods for fuorescent images are diferent without a proper pathways after complex peripheral nerve injuries [4]. comparison. Although almost all peripheral nerves are Terefore, the ability to identify and diferentiate motor a mixture of motor and sensory nerves, the facial nerve and sensory fascicles is greatly benefcial to the develop- is mainly composed of motor nerve fbers and the sural ment of new approaches to facilitate neural regeneration. nerve is mainly composed of sensory nerve fbers [17, In addition, the ability to identify motor and sensory fas- 18]. We hypothesize that preferable markers will be eval- cicles is crucial to the development of next generation uated and/or an optimal combination will be selected to nerve signal-controlled neuro-prosthetic limbs with sen- identify and diferentiate the motor and sensory axons sory feedback technology, which is connected to residual using immunofuorescence staining in this side by side peripheral nerves through the neural interface via intra- comparison in the facial and sural nerve. In this study, fascicular electrodes as we reported [5–7]. It’s particu- we selected the relatively pure facial and sural nerves as larly important to reliably distinguish motor and sensory either the motor or sensory fascicles for staining, and nerve fascicles to properly transmit signals via microelec- examined the expressions of available and commonly trode as motor order or sensory feedback via the regener- used motor markers [choline acetyltransferase (ChAT), ated nerves [7]. tyrosine kinase receptor A (TrkA)] and sensory mark- Currently, there are four reported methods to distin- ers [neuroflament protein 200 kDa (NF-200), calcitonin guish sensory and motor nerve fascicles: anatomical, gene-related peptide (CGRP) and Transient receptor electrophysiological, infrared spectrum, and enzymohis- potential vanillic acid subtype1 (TRPV1)] using immuno- tochemical staining [8–11]. Te anatomical method has fuorescence staining aiming to evaluate the best difer- been widely used in the past decades, but surgeons can entiative approach. Tese markers have been widely used only rely on their own experience to estimate the type of to label motor or sensory nerve fascicles experimentally nerve fascicle, and may cause partial or total loss of nerve [19, 20], however their quantifed preferential staining in function after nerve transplantation [12]. Terefore, peripheral nerves after peripheral nerve injury have not the anatomical technique alone is difcult to efectively been studied. gauge the type of fascicle. Electrophysiological methods such as evoked potentials were used to distinguish sen- sory from motor nerve fbers. While we have extensive Materials and methods experience with the electrophysiological study of nerve Experimental procedures injury [5, 6, 13, 14], this method can only distinguish the From 5 fresh euthanized nude rats, weighing 200 g to 250 main nerve branch; it is unable to show the composition g, we obtained healthy facial nerve and sural nerve speci- of the nerve fber. Moreover, there is a need for larger mens. To expose the facial nerve trunk and its branches, sample sizes to study the electrophysical technique due a 1 cm skin incision on a horizontal plane was performed to the high variance of measurements seen in current from the inferior margin of the auricular, extending ante- studies [15]. Infrared spectrum identifcation requires a riorly. Facial nerve specimens were obtained by transect- variety of equipment, complex calculations, and many ing at the stylomastoid foramen and 5 mm distal to the interference factors, which limits its application to a great skin incision, thus extracting a 10 mm nerve segment. A extent [10]. Enzymohistochemistry staining, including 1-cm long sural nerve segment was dissected from the immunofuorescence staining and immunohistochemi- sciatic nerve. We obtained both sides (10 facial nerve cal staining, is currently one of the most frequently used specimens and 10 sural nerve specimens) in all rats, and methods. However, it is difcult to distinguish the results randomly selected one side of each nerve type for the fol- using immunohistochemistry after labeling with a multi lowing studies. Diferentially expressed proteins could substrate color system. In addition, the color of the sub- be observed in proximal and distal nerve segments due strate and the thickness of the slice will afect the fnal to diferent cells and extracellular matrix of proximal and result, and the chromogenic substrate is an enzymatic distal nerve segments [21]. In our study, all the nerve sec- reaction that easily saturates the substrate, thus limit- tions were collected from the similar position of nerves. ing the semi quantitative analysis [16]. Compared with Experimental protocols were approved by the IACUC of Zhou et al. J Transl Med (2021) 19:207 Page 3 of 12 University of Maryland School of Medicine Animal Care Statistics and Use Committee.
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