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      A dysphagia model with denervation of the pharyngeal constrictor muscles in guinea pigs: functional evaluation of swallowing

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          Abstract

          Introduction

          Swallowing impairment is a crucial issue that can lead to aspiration, pneumonia, and malnutrition. Animal models are useful to reveal pathophysiology and to facilitate development of new treatments for dysphagia caused by many diseases. The present study aimed to develop a new dysphagia model with reduced pharyngeal constriction during pharyngeal swallowing.

          Methods

          We analyzed the dynamics of pharyngeal swallowing over time with the pharyngeal branches of the vagus nerve (Ph-X) bilaterally or unilaterally transected, using videofluoroscopic assessment of swallowing in guinea pigs. We also evaluated the detailed anatomy of the pharyngeal constrictor muscles after the denervation.

          Results

          Videofluoroscopic examination of swallowing showed a significant increase in the pharyngeal area during swallowing after bilateral and unilateral sectioning of the Ph-X. The videofluoroscopy also showed significantly higher pharyngeal transit duration for bilateral and unilateral section groups. The thyropharyngeal muscle on the sectioned side was significantly thinner than that on the intact side. In contrast, the thickness of the cricopharyngeal muscles on the sectioned and intact sides were not significantly different. The mean thickness of the bilateral thyropharyngeal muscles showed a linear correlation to the pharyngeal area and pharyngeal transit duration.

          Discussion

          Data obtained in this study suggest that denervation of the Ph-X could influence the strength of pharyngeal contraction during pharyngeal swallowing in relation to thickness of the pharyngeal constrictor muscles, resulting in a decrease in bolus speed. This experimental model may provide essential information (1) for the development of treatments for pharyngeal dysphagia and (2) on the mechanisms related to the recovery process, reinnervation, and nerve regeneration following injury and swallowing impairment possibly caused by medullary stroke, neuromuscular disease, or surgical damage from head and neck cancer.

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          Most cited references56

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          Dysphagia after stroke: incidence, diagnosis, and pulmonary complications.

          To determine the incidence of dysphagia and associated pulmonary compromise in stroke patients through a systematic review of the published literature. Databases were searched (1966 through May 2005) using terms "cerebrovascular disorders," "deglutition disorders," and limited to "humans" for original articles addressing the frequency of dysphagia or pneumonia. Data sources included Medline, Embase, Pascal, relevant Internet addresses, and extensive hand searching of bibliographies of identified articles. Selected articles were reviewed for quality, diagnostic methods, and patient characteristics. Comparisons were made of reported dysphagia and pneumonia frequencies. The relative risks (RRs) of developing pneumonia were calculated in patients with dysphagia and confirmed aspiration. Of the 277 sources identified, 104 were original, peer-reviewed articles that focused on adult stroke patients with dysphagia. Of these, 24 articles met inclusion criteria and were evaluated. The reported incidence of dysphagia was lowest using cursory screening techniques (37% to 45%), higher using clinical testing (51% to 55%), and highest using instrumental testing (64% to 78%). Dysphagia tends to be lower after hemispheric stroke and remains prominent in the rehabilitation brain stem stroke. There is increased risk for pneumonia in patients with dysphagia (RR, 3.17; 95% CI, 2.07, 4.87) and an even greater risk in patients with aspiration (RR, 11.56; 95% CI, 3.36, 39.77). The high incidence for dysphagia and pneumonia is a consistent finding with stroke patients. The pneumonia risk is greatest in stroke patients with aspiration. These findings will be valuable in the design of future dysphagia research.
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            Brain stem control of swallowing: neuronal network and cellular mechanisms.

            A Jean (2001)
            Swallowing movements are produced by a central pattern generator located in the medulla oblongata. It has been established on the basis of microelectrode recordings that the swallowing network includes two main groups of neurons. One group is located within the dorsal medulla and contains the generator neurons involved in triggering, shaping, and timing the sequential or rhythmic swallowing pattern. Interestingly, these generator neurons are situated within a primary sensory relay, that is, the nucleus tractus solitarii. The second group is located in the ventrolateral medulla and contains switching neurons, which distribute the swallowing drive to the various pools of motoneurons involved in swallowing. This review focuses on the brain stem mechanisms underlying the generation of sequential and rhythmic swallowing movements. It analyzes the neuronal circuitry, the cellular properties of neurons, and the neurotransmitters possibly involved, as well as the peripheral and central inputs which shape the output of the network appropriately so that the swallowing movements correspond to the bolus to be swallowed. The mechanisms possibly involved in pattern generation and the possible flexibility of the swallowing central pattern generator are discussed.
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              Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts.

              The aim of this study was to map the viscerotopic representation of the upper alimentary tract in the sensory ganglia of the IXth and Xth cranial nerves and in the subnuclei of the solitary and spinal trigeminal tracts. Therefore, in 172 rats 0.5-65 microliters of horseradish peroxidase (HRP), wheat germ agglutinin-HRP, or cholera toxin-HRP were injected into the trunks and major branches of the IXth and Xth cranial nerves as well as into the musculature and mucosa of different levels of the upper alimentary and respiratory tracts. The results demonstrate that the sensory ganglia of the IXth and Xth nerves form a fused ganglionic mass with continuous bridges of cells connecting the proximal and distal portions of the ganglionic complex. Ganglionic perikarya were labeled in crude, overlapping topographical patterns after injections of tracers into nerves and different parts of the upper alimentary tract. After injections into the soft palate, pharynx, esophagus, and stomach, anterograde labeling was differentially distributed in distinct subnuclei in the nucleus of the tractus solitarius (NTS). Palatal and pharyngeal injections resulted primarily in labeling of the interstitial and intermediate subnuclei of the NTS and in the paratrigeminal islands (PTI) and spinal trigeminal complex. Esophageal and stomach wall injections resulted in labeling primarily of the subnucleus centralis and subnucleus gelatinosus, respectively. The distribution of upper alimentary tract vagal-glossopharyngeal afferents in the medulla oblongata has two primary groups of components, i.e., a viscerotopic distribution in the NTS involved in ingestive and respiratory reflexes and a distribution coextensive with fluoride-resistant acid-phosphatase-positive regions of the PTI and spinal trigeminal nucleus presumably involved in visceral reflexes mediated by nociceptive or chemosensitive C fibers.
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                Author and article information

                Contributors
                URI : https://loop.frontiersin.org/people/2751429/overviewRole: Role: Role: Role: Role: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/2680840/overviewRole: Role: Role: Role: Role: Role: Role: Role: Role: Role: Role: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/2741732/overviewRole: Role: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/2761062/overviewRole: Role:
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                Journal
                Front Neurol
                Front Neurol
                Front. Neurol.
                Frontiers in Neurology
                Frontiers Media S.A.
                1664-2295
                19 June 2024
                2024
                : 15
                : 1401982
                Affiliations
                [1] 1Department of Otolaryngology-Head and Neck Surgery, Kyoto Prefectural University of Medicine , Kyoto, Japan
                [2] 2Department of Otolaryngology-Head and Neck Surgery, Faculty of Medicine, Saga University , Saga, Japan
                [3] 3Department of Otolaryngology-Head and Neck Surgery, Fukuoka Sanno Hospital , Fukuoka, Japan
                [4] 4Department of Speech and Hearing Sciences, International University of Health and Welfare, and the Voice and Swallowing Center, Fukuoka Sanno Hospital , Fukuoka, Japan
                Author notes

                Edited by: Teresa Pitts, University of Missouri, United States

                Reviewed by: Kimberly Iceman, University of Missouri, United States

                Alyssa Huff, Seattle Children’s Research Institute, United States

                *Correspondence: Yoichiro Sugiyama, yoichiro@ 123456cc.saga-u.ac.jp ; yoichiro99@ 123456me.com
                Article
                10.3389/fneur.2024.1401982
                11220121
                38962483
                6ae63fdf-5737-4777-b9e9-90a491089abe
                Copyright © 2024 Hashimoto, Sugiyama, Kaneko, Kinoshita, Yamamoto, Ishida, Umezaki and Hirano.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 16 March 2024
                : 06 June 2024
                Page count
                Figures: 4, Tables: 1, Equations: 0, References: 56, Pages: 9, Words: 6391
                Funding
                The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This work was supported by a Grant-in-Aid for Scientific Research (C) (Grant Numbers 22K09671, 23K15867, and 21K09613).
                Categories
                Neurology
                Original Research
                Custom metadata
                Neuromuscular Disorders and Peripheral Neuropathies

                Neurology
                dysphagia,swallowing,guinea pig,pharyngeal branch of the vagus nerve,videofluoroscopy
                Neurology
                dysphagia, swallowing, guinea pig, pharyngeal branch of the vagus nerve, videofluoroscopy

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