Quantitative assessment of oral and pharyngeal function in Parkinson's disease

Oral and pharyngeal dysfunction is common in Parkinson's disease. To reveal the frequency of swallowing dysfunction and correlate swallowing dysfunction with locomotor disturbances, we studied 75 patients with Parkinson's disease staged I–IV according to the Hoehn and Yahr score. We assessed oral and pharyngeal swallow during optimal medication by a quantitative test of swallowing (the ROSS test) measuring the suction pressure, bolus volume, swallowing capacity, and time for important events in the swallowing cycle. We found abnormal results in 7/12 patients (58%) in stage 1 of the Hoehn and Yahr score, in 13/14 patients (93%) in stage 2, in 29/32 patients (91%) in stage 3, and in 16/17 patients (94%) in stage 4. Abnormal test results in stages, 1, 2, and 3 were seldom related to swallowing difficulties noticed by the patients. In advanced disease (Hoehn and Yahr stage 4), the abnormal results were often considerable, with swallowing difficulties obvious to the patient. Two of 17 patients coughed during or immediately after the test and 3/17 patients were unable to complete the test. The degree of swallowing disturbance increased during stress (forced, repetitive swallow). The Hoehn and Yahr score and the results in the ROSS test did not correlate, indicating that swallowing disturbances are due to nondopaminergic degeneration. Silent swallowing impairment may interfere with the nutrition and quality of life in Parkinson's disease, thus it is of interest to monitor this in clinical practice.     

Oral function test for monitoring suction and swallowing in the neurologic patient

Disturbances in swallowing are common in neurologic disease but difficult to evaluate in the clinical setting. Fundamental variables such as bolus volume, swallow capacity (volume ingested over time), and the relation between ingestion and time for important events in oral and pharyngeal swallowing have not been sufficiently studied. We therefore employed a composite method for monitoring oral and pharyngeal swallowing function: the test of Repetitive Oral Suction Swallow (the ROSS test). The technical details are described as well as preliminary results from a pilot study of 20 healthy subjects and 5 patients with neurologic swallowing impairment. The correlation with respect to time sequences for major events in bolus ingestion and oral processing as monitored by the ROSS test and by videoradiography is explained. With this simple and rapid bedside test, the immediate and long-time result of therapeutic interventions in dysphagic patients may be monitored.     

Coordination of mastication and swallowing

The coordination of mastication, oral transport, and swallowing was examined during intake of solids and liquids in four normal subjects. Videofluorography (VFG) and electromyography (EMG) were recorded simultaneously while subjects consumed barium-impregnated foods. Intramuscular electrodes were inserted in the masseter, suprahyoid, and infrahyoid muscles. Ninety-four swallows were analyzed frame-by-frame for timing of bolus transport, swallowing, and phases of the masticatory gape cycle. Barium entered the pharynx a mean of 1.1 s (range −0.3 to 6.4 s) before swallow onset. This interval varied significantly among foods and was shortest for liquids. A bolus of food reached the valleculae prior to swallow onset in 37% of sequences, but most of the food was in the oral cavity at the onset of swallowing. Nearly all swallows started during the intercuspal (minimum gape) phase of the masticatory cycle. Selected sequences were analyzed further by computer, using an analog-to-digital convertor (for EMG) and frame grabber (for VFG). When subjects chewed solid food, there were loosely linked cycles of jaw and hyoid motion. A preswallow bolus of chewed food was transported from the oral cavity to the oropharynx by protraction (movement forward and upward) of the tongue and hyoid bone. The tongue compressed the food against the palate and squeezed a portion into the pharynx one or more cycles prior to swallowing. This protraction was produced by contraction of the geniohyoid and anterior digastric muscles, and occurred during the intercuspal (minimum gape) and opening phases of the masticatory cycle. The mechanism of preswallow transport was highly similar to the oral phase of swallowing. Alternation of jaw adductor and abductor activity during mastication provided a framework for integration of chewing, transport, and swallowing.     

Surface EMG measurements at the throat during dry and wet swallowing

Within the sphere of dysphagia management, there is a growing need for the development of noninvasive methods of quantification of swallowing disorders. The purpose of the present investigation was to determine if surface electromyogram (EMG) at the throat could be measured during swallowing. Surface EMG was measured from 35 normal human subjects during dry and wet swallowing. The EMG signals recorded were highpass filtered using digital fourth order highpass Butterworth filter to eliminate baseline variations. Spectral analysis was performed on the filtered signals. The mean power values of the surface EMG signals were then calculated. Paired t-test between the mean power values of surface EMG during dry and wet swallowing showed a statistically significant difference (p<0.005). The results of the study confirmed the hypothesis that surface EMG at the throat during swallowing could be measured. Mean power of surface EMG measurement provides a reliable noninvasive measure of swallowing.     

Dietary management of swallowing disorders

Two major concerns in the dietary management of the dysphagic patient are to maintain adequate nutrition and to ensure safety during oral feeding. Dysphagic patients require modifications of standard hospital diets. Kitchen or nursing staff must remove from standard diet trays solid foods and liquids that pose swallowing hazards. Training kitchen and nursing staff and removing food are time consuming. It is also hazardous if certain foods are served to dysphagic patients through error or lack of knowledge. In addition, there is risk of inadequate nutrition when food is removed from trays. This paper proposes a four-level diet plan for patients who have difficulty swallowing solids and liquids. These diets gradually advance for patients undergoing treatment to improve swallowing function. The proposed diets save time for kitchen and nursing staff, reduce the risk of aspiration among patients, and serve as models for families as they prepare for discharge and meal planning at home. Diet guidelines are based on recommendations of the American Dietetic Association.     

Manofluorographic analysis of swallowing in the elderly

This study examined the effect of aging on the mechanisms of swallowing by comparing 16 elderly subjects (80 years±5) with 20 healthy volunteers. Manofluorography was used to obtain quantitative and qualitative data of the pharyngeal swallow. Aging is associated with a significant decrease in the level of negative pressure resulting from the opening of the upper esophageal sphincter and with a substantial number of incomplete relaxations of the sphincter. In addition, several qualitative changes were noted.     

Volume accommodation during swallowing

Bolus volume is an important modifier of the biomechanical events of the oropharyngeal swallow. The biomechanical events comprising a swallow can be divided into events associated with the reconfiguration of the pharynx into a swallow pathway and events associated with bolus transport from the oropharynx into the esophagus. Volume modification is achieved differently for the events of reconfiguration and propulsion. In the case of reconfiguration, a longer time is allocated to the process, as exemplified by sustained laryngeal elevation and hyoid excursion during larger volume swallows. On the other hand, in the case of bolus expulsion, volume accommodation is accomplished within the same period of time by utilizing increased vigor of expulsion. The result of deglutitive volume accommodation is a remarkably different fluoroscopic appearance of a small vs. a large volume swallow. The larger volume swallow seemingly takes longer and results in much more vigorous bolus expulsion than a small volume. However, this is more related to the bolus than the swallow.     

Methodology for detecting swallowing sounds

The use of cervical auscultation in the evaluation of the pharyngeal swallow may become a part of the clinical evaluation of dysphagic patients. Though its use is based on subjective evaluation, an acoustic analysis of swallowing sounds might establish more objective criteria in the detection of swallowing disorders. The present study sought to investigate three aspects of the methodology for detecting swallowing sounds: (1) the type of acoustic detector unit suited to an acoustic analysis of the pharyngeal swallow, (2) the type of adhesive suited for the attachement of the detector, and (3) the optimal site for sound detection of the pharyngeal swallow. An accelerometer with double-sided paper tape was selected as the appropriate detector unit because of its wide range of frequency response and small attenuation level. Using this detector unit, swallowing sounds and noise associated with simulated laryngeal elevation and the carotid pulse were acquired at 24 sites on the neck in 14 normal subjects; these signals were acoustically analyzed. The determination of the optimal site for detecting swallowing sounds was based on the signal-to-noise ratio. The site over the lateral border of the trachea immediately inferior to the cricoid cartilage is the optimal site for detection of swallowing sounds because this site showed the greatest signal-to-noise ratio with the smallest variance. The site over the center of the cricoid cartilage and the midpoint between the site over the center of the cricoid cartilage and the site immediately superior to the jugular notch were also considered to be the most appropriate sites.     

Sounds of swallowing following total laryngectomy

Accelerometer transduced sounds of swallowing in total laryngectomees did not show acoustical differences for liquid vs paste swallows, as are found in normals. Compared with normal swallows, tongue propulsion of the bolus in laryngectomee swallows occurred closer in time to a distinctive spectral change associated with bolus flow into the esophagus. Interpretation stressed the lack of mechanical traction from laryngeal elevation contributing to pharyngoesophageal sphincter opening, and the increased role of tongue propulsion in laryngectomee swallows. Supported by grant no. CA 43838 from the National Cancer Institute     

Quantitative aspects of swallowing in an elderly nondysphagic population

The prevalence of swallowing impairment increases with age and is a major health care problem in the elderly. It has been assumed that age-related changes in nerves and muscles hamper muscle strength and coordination of swallowing. However, it is unclear what impairment is related to primary aging and what is the consequence of diseases prevalent in the elderly (secondary aging). In order to quantify swallowing in nondysphagic elderly we used the noninvasive ROSS (Repetitive Oral Suction Swallow) test. A total of 53 individuals aged 76±5 years (mean±SD) were examined. We found that the nondysphagic elderly demonstrated significant differences compared with young individuals in 10 of 17 measured variables, i.e., decreased peak suction pressure, increased frequency of multiple swallows after one ingestion, increased frequency of polyphasic laryngeal movements, increased frequency of inspiration after swallowing, and increased frequency of coughing during or after swallowing. Therefore, primary aging mainly seems to influence coordination of swallowing, but oral and pharyngeal swallow per se seem to be unaffected.     

Neurophysiology of swallowing in the aged

The neurophysiology of normal swallowing and its alterations related to age are reviewed. Clinical implications in health and disease are discussed.Presented in part at the Second Annual Scientific Meeting of the Dysphagia Research Society, October 22, 1993, Lake Geneva, WI, USA     

Masticatory ability in experimentally induced xerostomia

The masticatory ability of 15 nondysphagic volunteers with complete natural dentition was tested using different chewing parameters including preparation of a two-color plastic chewing gum (bolus shape, and color mixture), particle reduction of a piece of silicone, and number of strokes before swallow of almonds. The tests were performed under conditions of normal salivation and experimental oral dryness caused by intramuscular injection of methylscopolamine. The chewing gum tests as well as the silicone particle reduction tests were not influenced by lack of salivation. The number of chewing strokes prior to the initiation of swallowing of almonds was significantly increased. Oral dryness seems to cause accumulation of particles in the oral cavity from friable food and the particulate material is not transported posteriorly into a “readyto-swallow” positioning. The absorption of saliva by dry oral content such as an almond further impaired oral manipulation of food.     

An In Vitro Model for Studying Neuromuscular Transmission in the Mouse Pharynx

The muscles of the pharynx are controlled by networks of neurons under the control of specific regions in the brain stem, which have been fairly well studied. However, the transmission between these neurons and the pharyngeal muscles, at the motor end plates, is less well understood. Therefore, an in vitro model for the study of neuromuscular transmission in the pharyngeal muscle of the mouse was developed. Ring preparations from the inferior constrictor and the cricopharyngeus muscles were isolated and mounted for isometric force recording at physiologic temperature. Preparations from the diaphragm and the soleus muscles were examined in parallel. The muscles were stimulated at supramaximal voltage with short tetani at 100 Hz. Following direct stimulation of the muscle fibers, using a longer pulse duration, the rate of force development of the pharyngeal muscles was similar to that of the diaphragm and faster than that of the soleus muscle. By varying the duration of the stimulation pulses, conditions where the nerve-mediated activation contributed to a major extent of the contractile responses were identified. Gallamine completely inhibited the nerve-mediated responses. In separate experiments the dose dependence of gallamine inhibition was examined, showing similar sensitivity in the inferior pharyngeal constrictor compared to the diaphragm and soleus muscles. We conclude that reproducible contractile responses with an identifiable nerve-induced component can be obtained from the mouse inferior pharyngeal constrictor. The pharyngeal muscles have contractile characteristics similar to those of the faster diaphragm. The sensitivity to the neuromuscular blocking agent gallamine of the inferior pharyngeal constrictor was in the same concentration range as that of the diaphragm and soleus muscles.

Oropharyngeal swallowing after stroke in the left basal ganglion/internal capsule

One of the foci of Martin Donner's work was the neural control of swallowing. This present investigation continues that work by examining oropharyngeal swallowing in 8 patients identified with a single, small, left-basal ganglion/internal capsule infarction and 8 age-matched normal subjects. Stroke patients were assessed with a bedside clinical and radiographic swallowing assessment, and normal subjects received only the radiographic study. Results revealed disagreement between the bedside and radiographic assessments in one of the 8 stroke patients. Stroke and normal subjects differed significantly on some swallow measures on various bolus viscosities, but behaved the same as normal subjects on a number of measures. Differences in swallowing in the stroke subjects were not enough to prevent them from eating orally. The significant differences seen in the basal ganglia/intemal capsule stroke subjects may result from damage to the sensorimotor pathways between the cortex and brainstem. These differences emphasize the importance of cortical input to the brainstem swallowing center in maintaining the systematic modulations characteristic of normal swallowing physiology.     

Food intake by maneuver; An extreme compensation for impaired swallowing

We report two young patients able to exist on exclusively oral intake despite an absent pharyngeal swallow response. Videofluoroscopic swallowing studies showed that both patients used a sequence of devised maneuvers rather than a coordinated pharyngeal swallow to move the bolus, protect the airway, and open the upper esophageal sphincter during bolus ingestion. We conclude that it is possible for young, highly motivated individuals to maintain oral intake despite ablation of neurologic elements crucial for the normal swallow response.     

Periventricular white matter changes and oropharyngeal swallowing in normal individuals

Cranial magnetic resonance imaging (MRI) has revealed patchy periventricular white matter lesions or “unidentified bright objects” (UBOs) in otherwise neurologically intact individuals. Quantitative videofluoroscopic swallowing evaluations and cranial MRI examinations were studied in 49 neurologically normal volunteers (ages 43 to 79 years). Total swallowing duration (TSD) and its subcomponents of oral transit duration (OTD), stage transition duration (STD), and pharyngeal response duration were measured for liquid and semisolid swallows. MRIs were graded from 0, or no UBOs, to 3, or multiple and confluent lesions. The effect of the presence of UBOs on swallowing durational measures and risk factors was analyzed with age differences accounted for statistically (AN-COVA). TSD and OTD for semisolids were significantly differentiated by MRI score (P<0.009 andP<0.047, respectively). That is, a demonstrable effect was found for an increased number of UBOs on duration of oropharyngeal swallowing in normal individuals. Supported in part by The National Institute of Health (NS24427).     

Prevalence of Perceived Dysphagia and Quality-of-Life Impairment in a Geriatric Population

Dysphagia is an important problem for the elderly. While well characterized in acutely ill populations, the prevalence and quality-of-life changes associated with dysphagia remain poorly defined in the community geriatric population. This study recruited individuals 65 years and older from an independent-living facility. Two validated questionnaires were used: the M.D. Anderson Dysphagia Inventory (MDADI) and the general health Short Form-12 survey (SF-12v2^TM). Each participant also answered two questions: “Do you have difficulties with swallowing?” and “Do you think that swallowing difficulties are a natural part of aging?” Fifteen percent of subjects reported difficulties with swallowing. Of these, over half suffered substantial quality-of-life impairment in one or more domains of the MDADI. With respect to the second question, 23.4% of subjects believed dysphagia to be a normal part of aging, 37.4% did not. The SF-12v2 only weakly correlated with the MDADI in this population. In conclusion, there is a relatively high prevalence of dysphagia in the community-based geriatric population; significant quality-of-life impairment is a frequent finding. General health measures do not appear to be sensitive to swallowing-related quality of life. Finally, individuals may inaccurately ascribe swallowing problems to normal aging, supporting the role of community education about dysphagia in the elderly.     

The role of the cerebral cortex in swallowing

This paper reviews clinical, neuroanatomical, and neurophysiological studies that have implicated the cerebral cortex in the initiation and/or regulation of swallowing as well as related functions such as mastication. Cortical dysfunction has been reported to result in a variety of swallowing impairments. Furthermore, swallowing can be evoked and/or modulated by stimulation applied to restricted regions of the cortex. Neuroanatomical investigations and single neuron recording studies also provide some insights into the cortical structures, pathways, and mechanisms that may mediate deglutition.Studies referred to by the authors were supported by grant MT4918 to B.J.S. from the Medical Research Council of Canada     

The innervation of the human upper esophageal sphincter

The neuroanatomy and physiology of the human upper esophageal sphincter (UES) has long been controversial. As a result, there has been little progress in diagnosing and treating dysphagias involving this area. In this study, three specimens of the UES obtained from human autopsies were examined by Sihler's stain. This stain clears soft tissue while counterstaining the nerves, thereby allowing nerve supply to each muscle of the UES to be demonstrated. It was found that the nerve supply to each component of the UES is substantially different. The inferior pharyngeal constrictor (IPC) is supplied by a dense linear plexus which is about 1.0–1.5 cm wide and 10 cm long and located about 1.5 cm lateral to the attachment of the IPC on the thyroid lamina. The cricopharyngeal (CP) muscle receives its innervation from below via the recurrent laryngeal nerve (RLN) and from above via the pharyngeal plexus. Neural connections between the RLN and the pharyngeal plexus were observed. Finally, the upper esophagus (UE) is innervated by the RLN. The innervation pattern of each component of the UES suggests functional differences between these muscles. These observations help clarify the innervation of the UES. Accurate knowledge of the neuroanatomy of the UES is necessary for advances in diagnosis and treatment of pharyngeal dysphagia.     

Prevalence of swallowing complaints and clinical findings among 50–79-year-old men and women in an urban population

To determine the prevalence of swallowing and esophageal complaints in the general population, 300 men and 300 women were asked to answer a mailed questionnaire. The participation rate was 92.5%. Complaints were reported by 35%. The most common complaints were symptoms associated with gastroesophageal reflux (GER) and globus sensation, both with a rate of occurrence of 20%. Obstruction of the bolus reported by 3% was the individual symptom that most frequently brought patients to the doctor. To validate the questionnaire and to study possible organic causes behind these symptoms, 46 persons with symptoms were invited to undergo further examination. Cineradiography of the pharynx revealed that 7 of 14 patients with symptoms of GER had abnormalities in the esophagus. Eleven of 55 patients with GER symptoms at least once a week underwent endoscopy. One case of erosive esophagitis and one case of gastric ulcer were diagnosed. Four of nine patients with obstructive symptoms had defective closure of the laryngeal vestibule shown by cineradiography. Endoscopy in four patients with obstructive symptoms revealed benign findings. Thus, an epidemiologic study of patients with swallowing symptoms documented a low incidence of serious organic disease.