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ORIGINAL ARTICLE
Year : 2014  |  Volume : 4  |  Issue : 1  |  Page : 21-27

Cricopharyngeal dysfunction in lateral medullary syndrome


Department of Head and Neck Surgery, Amrita Institute of Medical Sciences, Kerala, India

Date of Web Publication22-Sep-2014

Correspondence Address:
C.S. Meera Priya
Swallowing Pathologist, Department of Head and Neck Surgery, Amrita Institute of Medical Sciences, Ponekkara, Cochin - 682 031, Kerala
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2230-9748.141461

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   Abstract 

Background: Dysphagia is a common consequence of medullary stroke, and it is particularly true in Lateral medullary syndrome (LMS). Aims: To compare the lateral medullary syndrome (LMS) to the middle cerebral artery infarct (MCA) population to study the swallowing dysfunction at the oral, pharyngeal, and esophageal level using flexible endoscopic evaluation of swallowing (FEES) and video-flouroscopic swallowing study (VFS). Materials and Methods: The swallowing characteristics in 16 patients (11 men and five women) with a mean age of 61.8 (range 44-78 years), with left LMS were compared with 18 patients (13 men and five women) with unilateral hemispheric infarction (left MCA), with a mean age of 58.2 (range 37-75). The swallowing characteristics were recorded and analysed. Results and Discussion: All LMS patients considered for this study had pharyngeal and proximal esophageal stage dysphagia. Swallowing difficulties noted were delayed pharyngeal swallow reflex, cricopharyngeal dysfunction, pooling in post-cricoid region (left > right side), and multiple swallows to clear bolus. All patients with L MCA infarct had difficulty with oral and pharyngeal stage dysphagia. All left MCA infarct patients showed delay in oral transit time, laryngeal penetration and aspiration. Conclusion: A substantial uniformity of pathophysiological characteristics was found. The pharyngeal and proximal esophageal stage of swallowing was affected in left LMS, but both oral and pharyngeal stage of swallowing was affected in left MCA infarct. Cricopharyngeal dysfunction was a typical finding in LMS, although severity varied. Because severe dysphagia is very common in stroke, active swallowing diagnostic and therapeutic approaches are needed.

Keywords: Cricopharyngeal dysfunction, lateral medullary syndrome, video flouroscopic swallowing assessment


How to cite this article:
Priya CM, Menon JR. Cricopharyngeal dysfunction in lateral medullary syndrome . J Laryngol Voice 2014;4:21-7

How to cite this URL:
Priya CM, Menon JR. Cricopharyngeal dysfunction in lateral medullary syndrome . J Laryngol Voice [serial online] 2014 [cited 2019 Apr 23];4:21-7. Available from: http://www.laryngologyandvoice.org/text.asp?2014/4/1/21/141461


   Introduction Top


Dysphagia affects up to half of stroke patients and promotes pneumonia and fatal outcome. [2],[3],[4] More than 70% of brainstem stroke patients had dysphagia and aspiration in VFSS. [4] Although dysphagia is a common consequence of stroke affecting brainstem, it is particularly true in the medullary stroke. [3],[4],[5]

The lateral medullary syndrome (LMS, Wallenberg's syndrome) is most often caused by occlusion of the intracranial segment of the vertebral artery (VA), which supplies the posterior inferior cerebellar artery. [6] Dysphagia has been reported in 51-94% of LMS patients. [7] The extent and severity of swallowing disorders can be considerably variable, i.e., very mild and transient in some but extremely severe and prolonged in others. It is known that dysphagia is more prominent and lasts longer in LMS patients than in hemispheric stroke patients. [8] It is reported in the literature that if dysphagia in stroke is recognized and treated early, the complications may be reduced, thereby increasing the functionality of the patients. [9]


   Materials and methods Top


The objectives of this study were to compare the left LMS to the left middle cerebral artery infarct (MCA) population to study the swallowing dysfunction at the oral, pharyngeal and esophageal level using the flexible endoscopic evaluation of swallowing (FEES) and video-flouroscopic swallowing study (VFS).

Participants

Sixteen stroke patients with LMS (11 men and 5women) and 18 left MCA infarct patients (13 men and five women) admitted in our hospital within first 3 months following stroke, having difficulty swallowing were the subjects in the present study. All these patients underwent emergency CT scan of the brain followed by MRI and magnetic resonance angiography (MRA). These radiological findings supported the presence of LMS and left MCA infarcts. All patients and their relatives were informed about the study and written consent was obtained at the beginning of the study.

The inclusion criteria used for patient selection were as follows:

  • Patients whose diagnosis being confirmed with radiographic imaging (CT/MRI) and clinical neurological assessments, as LMS and left MCA infarct
  • The presence of at least two of the six clinical aspiration risk markers (dysphonia, dysarthria, abnormal gag reflex, abnormal voluntary cough, cough during/after swallowing, and voice change after swallowing) [10],[11]
  • Patients with intact cognition and the ability to maintain upright posture at least with support
  • Patients having no contraindications to the exposure to radiations during videoflouroscopic procedures [Table 1].
    Table 1: The demographic details of acute dysphagia stroke patients including age/sex/history of pneumonia

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A bedside examination of swallowing (BDSE) was performed within first 2 weeks (10-14 days) after admission in 34 patients. Analysis of mental status, stroke severity lesion lateralization, prior interventions, communication status, voice quality, cranial nerves (V, VII, IX, X, XI, XII), evidence of coughing or choking, secretions, oral motor control, observation of swallowing on oral trial, control of the bolus in the oral phase, and patients perception of swallowing recovery was assessed (BDSE protocol given in appendix A).

The bedside screening test included swallowing 3 oz water and an oxygen (O 2 ) saturation evaluation with pulse oxymetry using second finger of the unaffected hand. Observations and recordings were made on how the water was swallowed; coughing/wet voice during or for 1 min after completion of swallow/water flow from the mouth and the presence of laryngeal elevation during or after water swallowing; and decreases in O 2 saturation by 2% and more were observed during/after swallowing. The abnormal parameters indicated a need for temporary tube feeding. The degree of severity of dysphagia graded using the BDSE is listed in the [Table 2].
Table 2: Dysphagia severity rating using BDSE

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In the present study, in all the 34 patients, the degrees of dysphagia were severe enough to necessitate non-oral feeding and dysphagia severity was scored as 2.

Procedure

After entering the demographic details, all patients were initially subjected to a flexible endoscopic evaluation of swallowing (FEES). The FEES test was performed by a speech language pathologist (SLP) under the guidance of otolaryngology practitioner using Karl storz nonducted fiberopticnasopharyngoscope, 3.4 mm in diameter, a light source, camera, and monitor and DVD recorder. FEES was performed with the patient in the sitting position. No local anesthetic agent was used to avoid its effects on palatal and pharyngeal functions. Before the procedure a lubricant gel was applied on the distal tip of nasopharyngoscope and an antifog agent was applied in the lens. The flexible scope was passed per nasally, slowly sliding the scope down. The assessment of anatomic and physiologic function of the oral and pharyngeal structures was assessed during pre-swallow and swallow observations. The parameters assessed during FEES were done according to protocol developed by Langmore [Table 3]. [12] Initially, the velopharyngeal closure, hypopharynx, base tongue, pharyngeal wall medialization, laryngeal elevation were evaluated without oral trial and was scored as normal/poor. In order to evaluate penetration, aspiration, and the presence of residue, 10 ml milk was used as liquid, 10 cc pudding as the semisolid and matchbox-sized biscuit as the solid food. The evaluation findings were recorded as video images and were analysed. The presence of residue was evaluated using Cricopharyngeal rating scale (CPRS) [Table 4].
Table 3: The parameters assessed during FEES developed by Langmore

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Table 4: The severity rating scale of cricopharyngeal dysfunction using CP dysfunction rating scale

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Then the entire patient was positioned to carry out VFSS. The instrument used for VFSS was Schimadzu videoflouroscope with VCR/Mini DV recorder and video monitor. The VFSS in this study was performed by a radiologist, along with an otolaryngologist, anesthetists and a speech language pathologist. Initially, a lateral view of videoflouroscopy followed byanteroposterior view was carried out. Patients stood during the examination, and the focus of the fluoroscopic image was defined anteriorly by the lips, superiorly by the hard palate, posteriorly by the posterior pharyngeal wall, and inferiorly by the bifurcation of the airway and esophagus (the seventh cervical vertebra). Different types and quantities of material were given during the lateral views. The material used was thin, thick and cookie coated with barium. The consistency which the patient had least difficulty was given initially. The patients were instructed to swallow each type of consistency in variable amounts. The patients were directed to swallow thin and thick bariumconsistencies in quantities of 3 and 5 mL (3 mL and 5 mL given with a syringe placed on the anterior portion of the oral cavity) and a match box sized cookie coated barium was given at the end. The entire clinical procedure was recorded on either three quarters or one half-inch video tape, with timing information encoded onto each frame to facilitate later frame-by-frame, slow motion examination to identify and define any possible swallowing disorders. Each subject's VFS was first analysed in slow motion to define any swallowing disorders, that is, visible swallowing abnormalities in bolus flow or structural movements displayed on each swallow. The parameters assessed during VFS were rated as normal/poor. The penetration and aspiration was scored using penetration - aspiration scale (PAS). [13] The parameters assessed were listed in the [Table 5].
Table 5: The stages of swallow and the parameters assessed in each stage using VFS

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Key components of the swallowing process were quantitively evaluated by use of the following measures:

  • Pharyngeal transit time: The time required for a bolus to move through the pharynx. This is measured from time the head of the bolus passes the ramus of mandible to the time the tail of the bolus passes through the upper oesophageal sphincter (UES)
  • Laryngeal penetration defined as entry of bolus into laryngeal vestibule but not below true vocal folds
  • Aspiration defined as the entry of the bolus below the true vocal folds.


Recording and scoring

Recording of each individual's swallowing was done while carrying out VFS and FEES and the data was saved for later analysis and observation notes were also taken as and when the recording was carried out.

Analysis

The analysis of the data was done by three judges who were speech-language pathologists by profession. The judges were kept blind with regard to the purpose of the study. These judges were selected from a group of five judges on the basis of the pilot study conducted wherein the judges were provided with the video recordings of subjects and response sheet to record the observation. Video recording of subject were randomly presented to the judges who were asked to analyse the recordings independently. A key which consisted of the descriptions of the various parameters in VFS and FEES was also included in the score sheet. The judges were expected to analyse the characteristics of the oral preparatory, oral and pharyngeal stages of swallowing in the two separate response sheets provide for VFSS and FEES procedures. They were permitted to rewind again until they were satisfied with identification of different parameters. Each of the judges had to carry out the analyses for all the 34 subjects.

Statistical analysis

Statistical analysis was done using IBM SPSS Statistics 20 Windows (SPSS Inc., Chicago, USA). For all the continuous variables, the results are either given in Mean ± SD or in Median (Range) and for categorical variables as percentage. To compare the mean of continuous variables between two groups, those following normal distribution, Independent sample t-test was used. To compare the averages of the continuous variables between two groups, those not following normal distribution, Mann-Whitney U test was performed. Parametric paired t-test and nonparametric Wilcoxon signed Rank Test was used for comparing paired observation. Pearson Chi Square test was used for finding the association between two categorical variables. The P < 0.05 were considered as statistically significant.


   Results Top


Our patients included 16 LMS patients (11 males and 5 females)[Group I] with a mean age of 57.88 and 18 left MCA infarct patients (13 males and 5 females) [Group II] with a mean age of 56.28. There was no significant difference between the age and sex of both the groups (P < 0.05). Statistical comparison of age was done using independent sample t test, while that of sex was done using Pearsons Chi-square test.

During the initial BDSE assessment, the parameters affected were statistically compared between the two groups. In left LMS, 11 (68.8%) of patients had intact motor function of the tongue at the oral preparatory phase, including coordinated bolus formation and mastication. Tongue movements were affected in 5 (31.2%) patients (deviated to left side). The palate movements were normal in 7 (43.8%) and reduced in the left side in 9 (56.2%) patients with uvula deviated to right were noted. The gag reflex was reduced in 7 (43.8) patients mostly in the left side and normal gag was noted in 9 (56.2%) patients [Table 6]. This ipsilateral paralysis noted in the structures were supported in the literature. [14]
Table 6: The comparison of parameters assessed during BDSE

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The statistical comparison of parameters assessed during BDSE and their levels of significance are given in [Table 6].

The FEES finding in LLMS patients was that, the pharyngeal stage of swallowing was predominantly affected in all the patients. The left vocal cord was paralysed with reduced laryngeal sensation and left pharyngeal wall medialization affected in 5 (31.2%) patients and normal in 11 (68.8%). Among the parameters compared, a significant difference (P < 0.05) was noted between the two groups in left vocal cord paralysis, left side pharyngeal wall medialization and laryngeal sensation. The anterior and vertical movements of larynx were reduced. Epiglottic deflection continuedto be absent, likely because of reduced vertical movement of larynx and posterior tongue. The major abnormality was with pharyngeal and upper esophageal sphincter (UES) function.

No contraction of the middle and inferior pharyngeal constrictors was evident in 5 (31.2%) left LMS patients, thereby rendering pharyngeal squeezeabsent at this level. The UES failed to open adequately, and as a consequence, the liquid and pureed bolus pooled in the hypopharynx with small amounts penetrating or aspirating into the upper airway. Severity of CP dysfunction for thick and thin consistencies was rated as three in 11 patients and two in five patients.

The VFS findings in LLMS patients were cricopharyngeal dysfunction, multiple swallowing to clear boluses from the pharynx to the esophagus, increased pyriform sinuses residue and aspiration from the pyriform sinuses. The penetration aspiration score (PAS) ranged from 4 to 8. Three patients did not sense the penetration but with prompting was able to reliably occlude the airway and expectorate the penetrated material back into the hypopharynx. Also with prompting, the patient was able to extend the elevation of the larynx in both range and time (Mendelsohn maneuver).

The results of FEES and VFS for patients with Left MCA infarct showed that the oral and pharyngeal stage of swallowing was affected. The CP dysfunction was rated as 0 in 12 patients and 1 in 6 patients. The PAS ranged from 3 to 8.

The PAS score was compared between Group I and II using Mann-Whitney U test, which shows no significant difference between both the groups [Figure 1].

The oral and pharyngeal transit times (OTT, PTT) and the severity of CP spasm for thin and thick barium has been compared between and within the group I and II. The OTT between groups was compared using independent t test and the PTT, CP spasm was compared using Mann-Whitney U test. The statistical analysis across group shows no significant difference for OTT [Table 7] but a significant difference was noted for PTT and CP spasm for thin and thick barium across groups (P > 0.05) [Figure 3] and [Table 8][Figure 2].
Table 7: OTT (thin and thick) barium across groups

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Table 8: PTT and CP spasm (thin and thick) barium across groups

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Figure 1: No signifi cant difference between PAS scores between group I and II

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Figure 2: Significant difference in PTT for thin and thick barium across the group I and II

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Figure 3: Significant difference in CP dysfunction severity for thin and thick barium across the group I and II

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The OTT and PTT for thin and thick barium was compared within the groups I and II. The OTT (thin and thick barium) within groups I and II was compared using paired sample test. The results of the statistical analysis showed that there is no significant difference between OTT for thin and thick barium within group I and II [Figure 4] and [Table 9].
Table 9: The comparison of OTT (thin and thick barium) within group I and II

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Figure 4: No significant difference for OTT within the groups for thin and thick barium

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The comparison of PTT (thin and thick barium) within group I and II was statistically analysed using Wilcoxon signed ranks test. The results showed that there is a significant difference (P < 0.05) between PTT for thin and thick bariums within the group [Figure 5].
Figure 5: A significant difference for PTT (Thin and thick barium) within the group

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   Discussion Top


Swallowing is a complex motor event. Central control of swallowing is regulated by a central pattern generator (CPG) positioned dorsally in the nucleus tractussolitarus and neighboring medullary reticular formation. The CPG serially activates the cranial nerve motor neurons, including the nucleus ambiguous and vagal dorsal motor nucleus, which then innervates muscles of deglutition. [14] Swallowing difficulties may occur following cortical or brainstem infarction especially infarction of the swallowing center in the rostral dorsolateral medulla which occurs in the lateral medullary infarction. [15]

Our study compared the left LMS population to the L MCA population to study the swallowing dysfunction at the oral, pharyngeal and esophageal level with the use of VFS and FEES. The major difference was in the reduced opening of UES (CP dysfunction) noted in all patients with left LMS which was not noticed in L MCA infarcts. At the neurological level, bilateral medullary swallowing centers function as one integrated center, and the infarction of a portion of this center is sufficient to cause complete loss of swallowing. [16] So, in the present case, though the patient had a small unilateral brainstem lesion, dysphagia was severe.

The opening of the UES depends on the appropriate relaxation of the cricopharyngeus muscle, movement of the larynx (upward and forward) during pharyngeal swallowing and bolus propulsion and bolus drive to open the sphincter. The complex sequence is considered to be under the control of medullary swallowing center in mammals. [17],[18],[19]

The aspiration of food material from pyriform sinuses residue after swallowing and multiple swallowing were observed on VFSS and FEES might be attributed to impaired UES opening. Impaired UES opening observed on VFSS and FEES may develop from weak pharyngeal contraction, failure of UES relaxation and incoordination between pharyngeal contraction and UES relaxation. [19] Logemann [20] hypothesized that the UES did not open and distend well in LMS due to decreased hyolaryngeal excursion and a lack of bolus pressure due to pharyngeal weakness, which was noted in our patient group also. Similar finding was noted by Martino et al. [15] who performed a manometric study in LMS patients and found that there is absent pharyngeal contraction at 1cm above UES, no effective relaxation of cricopharyngeous muscle, no swallow activity at the UES, no definite contractile activity at 6 cm of upper esophagus. [21],[22] These findings are compatible with a specific lesion of the connections from a programming CPG in the solitary tract nucleus to nucleus ambigous neurons, which supply the distal pharynx, upper esophageal sphincter, and proximal esophagus. There is functional preservation of the CPG control center in the nucleus tractussolitarus and of the vagal dorsal motor nucleus neurons innervating the smooth muscle of esophagus.

The second difference between two groups was related to the affected phase of the swallowing process. The pharyngeal and proximal esophageal of swallowing and laryngopharyngeal paralysis was predominantly encountered in left LMS, whereas both oral and pharyngeal phase of swallowing was affected in left MCA infarct patients. Outcomes of other researches in literature supported our finding. [15],[20],[23]


   Conclusions Top


The study proposed to compare the left LMS population to the left MCA population to study the swallowing dysfunction at the oral, pharyngeal and esophageal level. The pharyngeal and proximal esophageal stage dysphagia was seen in patients with left LMS, but both oral and pharyngeal stage was affected in left MCA infarct patients. Cricopharyngeal dysfunction was a common finding in patients with left LMS which was not noticed in left MCA infarct patients. Because dysphagia is only a symptom, knowledge of the characteristics of dysphagia is the only way to determine appropriate treatment. Until more research data are available to unequivocally characterize the swallowing mechanism abnormalities associated with stroke, VFS and FEES are necessary to tailor effective swallowing rehabilitation.

 
   References Top

1.Walter U, Knoblich R, Steinhagen V, Donat M, Benecke R, Kloth A. Predictors of pneumonia in acute stroke patients admitted to a neurological intensive care unit. J Neurol 2007;254:1323-9.  Back to cited text no. 1
    
2.Horner J, Buoyer FG, Alberts MJ, Helms MJ. Dysphagia following brain-stem stroke. Arch Neurol 1991;48:1170-3.  Back to cited text no. 2
    
3.Horner J, Massey EW, Brazer SR. Dysphagia after bilateral stroke. Neurology 1990;40:1686-8.  Back to cited text no. 3
    
4.Singh S, Hamdy S. Dysphagia in stroke patients. Postgrad Med J 2006;82:383-91.  Back to cited text no. 4
    
5.Horner J, Massey EW, Riski JE, Lathrop DL, Chase KN. Aspiration following stroke: Clinical correlates and outcome. Neurology 1988;38:1359-62.  Back to cited text no. 5
    
6.Martino R, Terrault N, Ezerzer F, Mikulis D, Diamant NE. Dysphagia in a patient with lateral medullary syndrome: Insight into the central control of swallowing. Gastroenterology 2001;121:420-6.  Back to cited text no. 6
    
7.Kim JS. Pure lateral medullary infarction: Clinical - radiological correlation of 130 acute, consecutive patients. Brain 2003;126:1864-72.  Back to cited text no. 7
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8.Ertekin C, Aydogdu I, Tarlaci S, Turman AB, Kiylioglu N. Mechanisms of dysphagia in suprabulbar palsy with lacunar infarct. Stroke 2000;31:1370-6.  Back to cited text no. 8
    
9.Martino R, Foley N, Bhogal S, Diamant N, Speechley M, Teasell R. Dysphagia after stroke: Incidence, diagnosis and pulmonary complications. Stroke 2005;36:2756-63.  Back to cited text no. 9
    
10.Daniels SK, Ballo LA, Mahoney MC, Foundas AL. Clinical predictors of dysphagia and aspiration risk: Outcome measures in acute stroke patients. Arch Phys Med Rehabil 2008;81:1030-3.  Back to cited text no. 10
    
11.Logemann JA. Manual for the video flouroscopic study of swallowing. Austin: Pro- Ed; 1993. p. 1-7.   Back to cited text no. 11
    
12.Langmore SE, Schatz K, Olsen N. Fiberoptic endoscopic examination of swallowing safety: A new procedure. Dysphagia 1988;2:216-9.  Back to cited text no. 12
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13.Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia 1996;11:93-8.  Back to cited text no. 13
    
14.Kim JS, Lee JH, Suh DC, Lee MC. Spectrum of lateral medullary syndrome. Correlation between clinical findings and magnetic resonance imaging in 33 subjects. Stroke 1994;25:1405-10.  Back to cited text no. 14
    
15.Martino R, Terrault N, Ezerzer F, Mikulis D, Diamant NE. Dysphagia in a patient with lateral medullary syndrome: Insight into central control of swallowing. Gastroenterology 2001;121:420-6.  Back to cited text no. 15
    
16.Aydogdu I, Ertekin C, Tarlaci S, Turman B, Kiylioglu N, Secil Y. Dysphagia in lateral medullary infarction (Wallenberg's Syndrome): An acute disconnection syndrome in premotor neurons related to swallowing activity? Stroke 2001;32:2081-7.  Back to cited text no. 16
    
17.Vigderman AM, Chavin JM, Kososky C, Tanmoush AJ. Aphagia due to pharyngeal constrictor paresis from acute lateral medullary infarction. J Neurol Sci 1998;155:208-10.  Back to cited text no. 17
    
18.Jean A. Brainstem organization of the swallowing network. Brain Behav Evol 1984;25:109-16.  Back to cited text no. 18
[PUBMED]    
19.Dick TE, Oku Y, Romaniuk JR, Cherniack NS. Interaction between central pattern generators for breathing and swallowing in the cat. J Physiol 1993;465:715-30.  Back to cited text no. 19
    
20.Logemann JA. Evaluation and treatment of swallowing Disorders. 2 nd ed. Austin: PRO ED; 1998. p. 1-7.  Back to cited text no. 20
    
21.Amri M, Car A. Projections from the medullary swallowing centre to the hypoglossal motor nucleus: A neuroanatomical and electrophysiological study in sleep. Brain Res 1988;441:119-26.  Back to cited text no. 21
    
22.Hila A, Castell JA, Castell DO. Pharyngeal and upper oesophageal sphincter manometry in the evaluation of dysphagia. J Clin Gasteroenterol 2001;33:355-61.  Back to cited text no. 22
    
23.Chiti-Batelli S, Delap T. Lateral medullary infarct presenting as acute dysphagia. Acta Otolaryngol 2001;121:419-20.  Back to cited text no. 23
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9]



 

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