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Abnormal patterns of breathing during swallowing in neurological disorders.

Swallowing momentarily inhibits breathing, and normally the great majority of apnoeas which accompany a swallow are followed by expiration (xE swallows). This swallowing-breathing interaction is regarded as one of several mechanisms by which the airway is protected from aspiration during swallowing. The purpose of this study was to investigate the interaction of breathing and swallowing in two groups of neurological patients. Twenty-two patients with defined neurological disorders involving various structures or pathways (brain, spinal cord and peripheral nerves) were studied to determine whether particular lesions resulted in breakdown of the normal breathing pattern (22 normal subjects were also assessed and their breathing-swallowing pattern was compared with that of neurological patients). Subsequently, 32 patients with motor neurone disease (MND) were studied to identify factors associated with an abnormal pattern (i.e. swallow apnoeas followed by inspiration) and to clarify whether an abnormal pattern is related to chest infections, episodes of coughing and choking during meals, and prognosis. The swallow apnoea in patients with brain, spinal cord and peripheral neurological diseases was followed by inspiration more frequently than expected [20/22 (91%) patients compared with 2/22 (9%) of normal subjects, P: < 0.001], but this was not associated with a specific site of lesion(s). However, patients with corticobulbar involvement tended to have post-apnoea inspiration more often than those without. MND patients commonly displayed an abnormal pattern during swallowing [14/32 (44%) patients] characterized by inspiration after swallow, prolonged swallow apnoea and multiple swallows per bolus. Over the period of follow-up (12-18 months) this pattern did not predict chest infections, coughing and choking episodes during meals or survival. It seems likely that post-swallowing apnoea inspiration is a non-specific concomitant of disordered swallowing and/or breathing rather than being an important mechanism of aspiration per se or of symptom production.

Adult↗

Functional properties of neurons in the primate tongue primary motor cortex during swallowing.

Recent studies conducted in our laboratory have suggested that the tongue primary motor cortex (i.e., tongue-MI) plays a critical role in the control of voluntary tongue movements in the primate. However, the possible involvement of tongue-MI in semiautomatic tongue movements, such as those in swallowing, remains unknown. Therefore the present study was undertaken in attempts to address whether tongue-MI plays a role in the semiautomatic tongue movements produced during swallowing. Extracellular single neuron recordings were obtained from tongue-MI, defined by intracortical microstimulation (ICMS), in two awake monkeys as they performed three types of swallowing (swallowing of a juice reward after successful tongue task performance, nontask-related swallowing of a liquid bolus, and nontask-related swallowing of a solid bolus) as well as a trained tongue-protrusion task. Electromyographic activity was recorded simultaneously from various orofacial and laryngeal muscles. In addition, the afferent input to each tongue-MI neuron and ICMS-evoked motor output characteristics at each neuronal recording site were determined. Neurons were considered to show swallow and/or tongue-protrusion task-related activity if a statistically significant difference in firing rate was seen in association with these behaviors compared with that observed during a control pretrial period. Of a total of 80 neurons recorded along 40 microelectrode penetrations in the ICMS-defined tongue-MI, 69% showed significant alterations of activity in relation to the swallowing of a juice reward, whereas 66% exhibited significant modulations of firing in association with performance of the trained tongue-protrusion task. Moreover, 48% showed significant alterations of firing in relation to both swallowing and the tongue-protrusion task. These findings suggest that the region of cortex involved in swallowing includes MI and that tongue-MI may play a role in the regulation of semiautomatic tongue movement, in addition to trained motor behavior. Swallow-related tongue-MI neurons exhibited a variety of swallow-related activity patterns and were distributed throughout the ICMS-defined tongue-MI at sites where ICMS evoked a variety of types of tongue movements. These findings are consistent with the view that multiple efferent zones for the production of tongue movements are activated in swallowing. Many swallow-related tongue-MI neurons had an orofacial mechanoreceptive field, particularly on the tongue dorsum, supporting the view that afferent inputs may be involved in the regulation of the swallowing synergy.

Animals↗

Modulation of laryngeal responses to superior laryngeal nerve stimulation by volitional swallowing in awake humans.

Laryngeal sensori-motor closure reflexes are important for the protection of the airway and prevent the entry of foreign substances into the trachea and lungs. The purpose of this study was to determine how such reflexes might be modulated during volitional swallowing in awake humans, when persons are at risk of entry of food or liquids into the airway. The frequency and the amplitude of laryngeal adductor responses evoked by electrical stimulation of the internal branch of the superior laryngeal nerve (ISLN) were studied during different phases of volitional swallowing. Subjects swallowed water on command while electrical stimuli were presented to the ISLN at various intervals from 500 ms to 5 s following the command. Laryngeal adductor responses to unilateral ISLN stimulation were recorded bilaterally in the thyroarytenoid muscles using hooked wire electrodes. Early ipsilateral R1 responses occurred at 17 ms, and later bilateral R2 began around 65 ms. The muscle responses to stimuli occurring during expiration without swallowing were quantified as control trials. Responses to stimulation presented before swallowing, during the swallow, within 3 s after swallowing, and between 3 and 5 s after a swallow were measured. The frequency and amplitude of three responses (ipsilateral R1 and bilateral R2) relative to the control responses were compared across the different phases relative to the occurrence of swallowing. Results demonstrated that a reduction occurred in both the frequency and amplitude of the later bilateral R2 laryngeal responses to electrical stimulation for up to 3 s after swallowing (P = 0.005). The amplitude and frequency of ipsilateral R1 laryngeal responses, however, did not show a significant main effect following the swallow (P = 0.28), although there was a significant time by measure interaction (P = 0.006) related to reduced R1 response amplitude up to 3 s after swallowing (P = 0.021). Therefore, the more rapid and shorter unilateral R1 responses continued to provide some, albeit reduced, laryngeal protective functions after swallowing, whereas the later bilateral R2 responses were suppressed both in occurrence and amplitude for up to 3 s after swallowing. The results suggest that R2 laryngeal adductor responses are suppressed following swallowing when residues may remain in the laryngeal vestibule putting persons at increased risk for the entry of foreign substances into the airway.

Adult↗

Swallowing function and medical diagnoses in infants suspected of Dysphagia.

OBJECTIVE: There has been an increase in infant swallowing disorders as a result of improved survival for infants born prematurely or with life-threatening medical disorders. These infants often have multiple health issues and an increased risk of respiratory complications. However, there is little understanding of the biomechanics of infant swallowing disorders. Therefore, the objectives of this study were to determine 1) the percentage of dysphagic infants who experience laryngeal penetration, aspiration, or nasopharyngeal backflow; 2) reasons for laryngeal penetration/aspiration; 3) whether infants with laryngeal penetration/aspiration clear their airway; and 4) the relationship between swallowing disorders and medical diagnoses. METHODS: Patients included 43 infants who were referred for videofluoroscopic swallowing studies in a university-affiliated pediatric medical center. Medical charts were reviewed. The videofluoroscopic swallowing studies were recorded on videotape, and each swallow was analyzed for laryngeal penetration, aspiration, nasopharyngeal backflow, cough, airway clearance, and reason for penetration/aspiration. Statistics included chi2 for nonparametric data and measures of central tendency for numeric/timing data. RESULTS: More than half of the infants experienced laryngeal penetration, aspiration, or nasopharyngeal backflow; however, the first occurrence of these events was after multiple swallows. Only 3 infants experienced laryngeal penetration and aspiration on the first swallow and all 3 had an absent pharyngeal response. Premature infants experienced significantly more nasopharyngeal backflow. Material in the pyriform sinuses before pharyngeal swallowing was associated with penetration/aspiration. In episodes of laryngeal penetration, all patients were able to clear their airway during the swallow without a cough. Almost all infants (8 of 9) who aspirated did not cough or clear their airway. CONCLUSIONS: This study demonstrated that most infants suspected of dysphagia showed overt abnormalities: laryngeal penetration, aspiration, and/or nasopharyngeal backflow on the videofluoroscopic swallowing study. Most of these infants did not demonstrate abnormalities in the first few swallows but displayed deterioration in swallowing function as they continued to feed. Thus, radiographic assessments in infants must examine multiple swallows. The high incidence of silent aspiration demonstrates the necessity of a videofluoroscopic assessment to evaluate swallowing function in these infants.

Biomechanical Phenomena↗

Coordination of suck-swallow-respiration in infants born to mothers with drug-abuse problems.

To delineate quantitatively differences in suck-swallow-respiration coordination during feeding in term infants exposed to drugs in utero, 16 control infants (10 females, six males; mean birthweight 3209g, standard error of the mean [SEM] 103g) and 15 drug-exposed infants (seven females, eight males; seven cocaine, eight opiates; neonatal abstinence [Finnegan] scores less than 10; mean birthweight 3001g, SEM 93g) were studied in the first three days of life and again at one month of age. Coefficients of variation (COVs) of suck-suck, swallow-swallow, and breath-breath intervals were used as measures of stability of individual rhythms. COVs of suck-swallow and swallow-breath intervals were used to determine stability of multiply integrated rhythms. In the first three days of life, a significantly higher percentage of 'apneic swallows' (runs of three or more swallows not associated with breathing movements, divided by total run-swallows) was noted during feeding in the drug-exposed infants (mean 5.3% SEM 1.7%) compared with controls (mean 0.9%, SEM 0.4%;p<0.02), who also had less breath-breath rhythmic stability (higher COV) and shorter swallow-breath intervals. These differences were no longer evident at one month of age. Opiate-exposed infants were generally more affected than the cocaine-exposed infants. Swallowing was less rhythmic in the drug-exposed cohort, especially in opiate-exposed infants, but this difference also disappeared by one month. In the first days of life, drug-exposed infants were less efficient feeders, ingesting less volume per run-swallow than controls (mean 0.31ml, SEM 0.05ml, versus 0.45ml, SEM 0.05ml;p<0.05). The decreased efficiency appeared to be compensated for by a slightly faster swallow rate (mean 53 swallows per minute SEM 2 versus 47 swallows per min, SEM 1, in controls;p<0.005). By one month of age these differences between groups had disappeared as well. Intrauterine drug exposure, even in infants with relatively mild symptoms of withdrawal, may adversely impact development of brainstem respiratory and swallow centers, thus affecting, albeit transiently, the underlying biorhythms of feeding.

Deglutition↗

3D volume-selective turbo spin echo for carotid artery wall imaging with navigator detection of swallowing.

PURPOSE: To improve 3D volume-selective turbo spin echo (TSE) carotid artery wall imaging by incorporating navigators to reduce artifacts caused by swallowing. MATERIALS AND METHODS: Images were acquired on a Siemens Magnetom Sonata 1.5T scanner. 3D volume-selective TSE scans of the carotid arteries were acquired in six healthy volunteers. A cross-pair navigator placed on the back of the tongue was used to detect swallowing and movement. Two swallowing patterns were tested: 1) a single swallow approximately halfway through the scan time, at the center of k(z), and 2) repeated swallowing as often as possible throughout the scan period. Images were acquired with and without navigators for comparison. Signal intensity in the lumen was quantified for the quality of blood suppression, and the clarity of the vessel wall in the common carotid was ranked by four independent blinded observers. RESULTS: In general, lower signal intensity was recorded in the lumen, and decreased blurring and ghosting were observed on scans with navigator control. This reduction in lumen signal intensity signifies an improvement in the black-blood imaging technique. The differences likely reflect the improved double inversion/blood suppression efficiency due to cycles being rejected when the heart rate changed at the point of swallowing, or decreased motional blurring/ghosting of tissue when the navigator is used, or a combination of these two effects. A statistical analysis of image quality showed a significant difference between navigated and non-navigated scans as scored by four independent, blinded observers. For both swallowing patterns, the mean score for the navigator images was on average 0.6 greater than that of non-navigator images (on a scoring scale of 0-5, where 0 = no vessel visible, and 5 = good delineation and blood suppression) and P-values for all observers were less than 0.01. Overall, the central swallow scans were scored higher than the repeated swallow scans. One reason for this may be the fact that the heart rate increased on swallowing, and this often lasted for one or two cardiac cycles after the navigator returned to the normal acceptance position. The effect of the increased heart rate after swallowing is likely to have an effect on double inversion blood suppression efficiency. Therefore, the increased amount of heart rate changes with repeated swallowing may have a greater adverse effect, even if the navigator rejects data views during the swallowing motion. CONCLUSION: The clarity of vessel wall delineation and the apparent efficiency of blood suppression are reduced by swallowing during acquisition. Both motion blurring and quality of blood suppression are factors that can be improved with the use of a navigator accept/reject method.

Artifacts↗

Swallowing dysfunction in infants less than 1 year of age.

BACKGROUND: Gastroesophageal reflux (GER) occurs frequently in infants and children and is implicated as a trigger for reactive airways disease. While evaluating patients for GER by upper gastrointestinal studies (UGI), we frequently noticed laryngeal penetration or tracheal aspiration in infants < 1 year of age. We conducted this prospective study to assess the incidence of swallowing dysfunction in infants with vomiting or respiratory symptoms. METHODS: Between February 1994 and August 1997, 1,003 UGI in infants < 1 year of age were performed by two experienced pediatric radiologists. Fluoroscopy of swallowing using an appropriate image intensifier was observed as part of the UGI in all patients. In addition to evaluating premature infants, former premature infants, and infants with underlying conditions such as bronchopulmonary dysplasia (BPD), congenital heart disease (CHD), esophageal atresia and/or tracheoesophageal fistula (EA), and neurologic disorders, we assessed swallowing in 472 full-term infants in the general population who had respiratory symptoms or suspected GER, but no other apparent abnormalities. Swallowing was not assessed in patients with congenital bowel obstruction. The presence of normal swallowing or swallowing dysfunction was recorded immediately following the study. Chest radiographs obtained on the same day as the UGI were evaluated in the study. Forty-four videotaped modified barium-swallow studies (MBSS) were obtained in 25 general-population infants and reviewed frame-by-frame to determine the length of time that barium could be visualized in the subglottic trachea. RESULTS: The incidence of swallowing dysfunction is significant in premature and former premature infants, those with BPD, CHD, EA, various syndromes, and neurologic abnormality. In the general population of full-term infants referred for evaluation of vomiting or respiratory symptoms, 63 (13.4 % of 472) had swallowing dysfunction. Forty-four had tracheal aspiration (TA) and 19 had laryngeal penetration (LP). Gastroesophageal reflux was found in 79.5 % with TA and in 68.4 % with LP. The MBSS confirmed swallowing dysfunction in all patients shown to have vocal cord penetration or tracheal aspiration by UGI. CONCLUSIONS: Careful evaluation of swallowing during an UGI can identify swallowing dysfunction in full-term infants who have respiratory problems, as well as in infants with an abnormality that predisposes the patient to aspiration. Episodes of tracheal aspiration may be fleeting and overlooked if swallowing is not assessed carefully. An MBSS can confirm the observation of swallowing dysfunction found during an UGI and assist in planning appropriate dietary therapy that minimizes the likelihood of tracheal aspiration during feeding.

Deglutition Disorders↗

Control of the central swallowing program by inputs from the peripheral receptors. A review.

Swallowing is a complex motor sequence, usually divided into a buccopharyngeal stage (coordinated contractions of several muscles of the mouth, pharynx and larynx) and an esophageal stage, called primary peristalsis. This motor sequence depends on the activity of medullary interneurons belonging to the swallowing center which program through excitatory and inhibitory connections the sequential excitation of motoneurons and vagal preganglionic neurons responsible for the whole motor sequence. The activity of the medullary swallowing neurons can occur without feedback phenomena: it is truly a central activity indicating that swallowing depends on a central network which may function without afferent support. However, the swallowing neurons receive a strong afferent input suggesting the involvement of sensory feedbacks during swallowing. The swallowing neurons present a short latency activation on electrical stimulation of the peripheral afferent fibers supplying the region of the tract which is under their control. In addition, the neurons are activated by localized distensions of the swallowing tract, this distension having to be done more and more distally when the neuronal discharge occurs later and later during swallowing. Furthermore the swallowing discharge of the central neurons is increased either when a bolus is swallowed or during a slight distension of the corresponding region of the tract. Thus, under physiological conditions, swallowing neurons receive sensory information from pharyngeal and esophageal receptors and the central program may be modified by peripheral afferents that adjust the motor sequence to the size of the swallowed bolus. The inputs from the peripheral receptors can also exert inhibitory effects depending on the central connections between the swallowing neurons.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗

Surface electromyographic studies of swallowing in normal children, age 4-12 years.

OBJECTIVES: Surface electromyographic (sEMG) studies were performed on 100 normal children, age 4-12 years, to establish normative database for duration and amplitude of muscle activity during swallowing and continuous drinking. STUDY DESIGN: Prospective observational study of healthy volunteers. METHODS: Parameters evaluated during swallowing include the timing and amplitude (in microV) of activity of m. orbicularis oris, masseter, submental and infrahyoid (laryngeal strap muscles (LSM)) groups covered by platisma. Four tests were examined: voluntary single swallows of saliva ("dry" swallow), voluntary single water swallows as normal, voluntary single swallows of excessive amount of water (up to 15ml), continuous drinking of 50ml of water (duration and number of swallows). Duration of muscle activity during swallowing (mean plus standard deviation (S.D.)) was measured for two age groups: 4-8 and 9-12 years old. The group of 40 adults, age 18-30 years, was taken as a control group. RESULTS: Normative data for duration and amplitude of muscle activity during single swallowing and continuous drinking are established for healthy children. The duration of muscle activity during swallows and drinking in all tests showed decrease with the age, and this tendency is statistically significant (one-dimensional analysis of variance, SPSS, chi(2) criterion, 95% confidence interval). There was no statistically significant difference in amplitude (range) measurements between children and adults (P=0.05). There was no statistically significant difference between male and female children duration of muscle activity during single swallowing and continuous drinking in all age groups (P>/=0.05). CONCLUSION: Surface EMG of swallowing is a simple and reliable noninvasive method for screening evaluation of swallowing with low level of discomfort of the examination. The normative timing of events data can be used for evaluation of complaints and symptoms, as well as for comparison purposes in pre- and postoperative stages and in electromyography (EMG) monitoring during ENT or neurological treatment. These parameters represent normal deglutition, and can be used to identify abnormalities in pediatric patients, and provide a basis for comparison of swallowing performance, both within and between patients.

Adolescent↗

Surface electromyographic studies of swallowing in normal subjects: a review of 440 adults. Report 2. Quantitative data: amplitude measures.

OBJECTIVES: Surface electromyographic (EMG) studies were performed on 420 normal adults to establish normative database for muscle activity's amplitude during swallowing and drinking clinically useful for ENT department. STUDY DESIGN: Prospective observational study of healthy volunteers. METHODS: Parameters evaluated during swallowing include the EMG activity of the orbicularis oris, masseter, submental, and infrahyoid muscle groups covered by platysma (range, mean, SD). Four tests were examined including voluntary swallow of saliva ("dry" swallow), voluntary single water swallows as normal (variable volume of a bolus), voluntary single swallows of fixed amount of water (20 mL), and continuous drinking of 100 mL of water. Activity of the above-mentioned muscles during swallowing was measured for groups of adults of different age groups. Groups included volunteers and were separated into age groups as follows: ages 18-30, 31-40, 41-50, 51-60, 61-70, and 70+ years of age. RESULTS: Normative data for electric muscle activity (mean +/- SD; range, in microV) during single swallowing and continuous drinking are established for healthy adults. The range of submental group activity during swallows showed a significant decrease with the age, whereas the range of masseter activity changed insignificantly (1-dimensional analysis of variance, SPSS, Chi-square criterion, 95% confidence interval). There were no significant changes in mean muscle activity between different age groups. These parameters represent activities required for normal deglutition, and can be used to identify abnormalities in ENT patients, and provide a basis for comparison of swallowing performance both within and between patients. These measurements can be performed in a simple way, cause no discomfort, do not use radiation, and are noninvasive. The relevance and clinical utility of new and alternative measures, in particular, are discussed. CONCLUSIONS: In single swallow tests range of electric activity of involved muscles is more informative than its mean. In the continuous drinking test, the mean electric activity is the only electric variance that can be evaluated. Orbicularis oris muscle activity is not important when reflex phase of a swallow is evaluated. Surface EMG of swallowing is a simple and reliable method for evaluation of swallowing with a low level of discomfort during the examination. The method can be easily used in outpatient ENT departments for quick evaluation of patients. The normative amplitude data can be used for comparison purposes in preoperaive and postoperative stages and in EMG monitoring during ENT treatment.

Adolescent↗

Maturational changes in the rhythms, patterning, and coordination of respiration and swallow during feeding in preterm and term infants.

To study the coordination of respiration and swallow rhythms we assessed feeding episodes in 20 preterm infants (gestational age range at birth 26-33wks; postmenstrual age [PMA] range when studied 32-40wks) and 16 term infants studied on days 1 to 4 (PMA range 37-41wks) and at 1 month (PMA range 41-45wks). A pharyngeal pressure transducer documented swallows and a thoracoabdominal strain gauge recorded respiratory efforts. Coefficients of variation (COVs) of breath-breath (BR-BR) and swallow-breath (SW-BR) intervals during swallow runs, percentage of apneic swallows (at least three swallows without interposed breaths), and phase of respiration relative to swallowing efforts were analyzed. Percentage of apneic swallows decreased with increasing PMA (16.6% [SE 4.7] in preterm infants 35wks; 1.5% [SE 0.4] in term infants; p<0.001). Term infants had significantly lower BR-BR COV (0.405 [SE 0.016]) than preterm infants (0.641 [SE 0.052] at >35wks' PMA; 0.693 [SE 0.059] at <or=35wks' PMA). Phase relation between swallowing and respiration stabilized with increasing PMA, with decreased apnea, and a significant increase in percentage of swallows occurring at end-inspiration. These data indicate that unlike the stabilization of suck and suck-swallow rhythms, which occur before about 36 weeks' PMA, improvement in coordination of respiration and swallow begins later. Coordination of swallow-respiration and suck-swallow rhythms may be predictive of feeding, respiratory, and neurodevelopmental abnormalities.

Analysis of Variance↗

Ovine fetal swallowing: expression of preterm neurobehavioral rhythms.

OBJECTIVE: Fetal swallowing contributes importantly to amniotic fluid volume regulation and fetal gastrointestinal maturation. Near-term ovine fetal swallowing occurs in discrete bouts of activity (at approximately 30-min intervals) in association with fetal electrocortical voltage changes. Thus, swallowing rhythms have been hypothesized to be entrained to fetal neurobehavioral states. In the preterm ovine fetus, electrocortical activity does not demonstrate differentiation into high- and low-voltage periods until 120-130 days' gestation. We sought to quantify patterns of preterm (114 days, 0.75 gestation) ovine fetal swallowing activity and volume, and, in view of the lack of electrocortical pattern changes, to explore whether swallowing activity was regulated by an independent central pacemaker. METHODS: Six singleton ovine pregnancies were chronically prepared with fetal and maternal femoral artery and vein catheters. Biparietal electrocortical electrodes were placed on the fetal skull. Following a minimum 5-day recovery period, fetuses were studied at 114 +/- 1 days. Patterns of fetal swallowing behavior were quantified by computer analysis of laryngeal-esophageal electromyography (EMG) and thoracic esophageal fluid flow during a 12-h period. RESULTS: Esophageal fluid flow was bidirectional, although antegrade flow predominated, leading to an average fluid acquisition rate of 13 +/- 3 ml/h (7.3 +/- 1.8 ml/h per kg) during the 12-h study (302 +/- 87 ml/day). Propagated esophageal EMG activity, representing coordinated 'swallows', averaged 56 +/- 6 swallows/h and correlated well with net esophageal fluid flow. 'Bouts' of swallowing activity (> or = 3 swallows/min) averaged 9 +/- 1 swallows/bout, lasted 1.8 +/- 1.4 min and accounted for 31 +/- 4% of the swallowed volume. Despite the absence of fetal electrocortical high-voltage/low-voltage transitions, there was a 26.1 +/- 3.9-min interval between periods of swallowing bout activity. CONCLUSIONS: Preterm (0.75 gestation) ovine fetal volume swallowed (302 ml/day) and volume swallowed for body weight (175 ml/day per kg) was significantly less than that previously noted at 0.85 gestation (831 ml/day, 274 ml/day per kg, respectively; p < 0.05) although the rates of swallowing activity were similar. The presence of swallowing bout activity at periodic intervals, in the absence of electrocortical differentiation, suggests an intrinsic central pacemaker regulating preterm fetal neurobehavior.

Animals↗

The influence of chemical gustatory stimuli and oral anaesthesia on healthy human pharyngeal swallowing.

This study explored the effects of taste and oral anaesthesia on human sequential swallowing. Subjects were healthy adults (n = 42, mean age 28 years, 21 females), investigated by means of a water swallow test. Taste stimuli comprised quinine, glucose, citrus and saline solutions compared with neutral water. Oral anaesthesia comprised topical lidocaine at doses of 10, 20 and 40 mg and compared with placebo. Data were collected on swallowing speed (volume per second), inter-swallow interval and swallowing capacity (volume per swallow). Compared with water, glucose, citrus and saline reduced swallowing speed (10.94 +/- 0.89 versus 9.56 +/- 0.79, 9.33 +/- 1.19, 9.37 +/- 0.92 ml/s respectively, P < 0.05). Inter-swallow interval was increased only by quinine and saline (1.47 +/- 1.11 versus 2.13 +/- 0.34 and 1.92 +/- 0.31 s, P < 0.04). Swallowing capacity was only marginally increased by quinine (P = 0.0759). Compared with the placebo, only 40 mg of lidocaine altered swallowing, immediately reducing the swallowing speed (7.89 +/- 2.34 versus 10.11 +/- 3.26 ml/s, P < 0.05) and increasing inter-swallow interval (1.67 +/- 0.38 versus 1.45 +/- 0.29 s, P < 0.01) without affecting capacity. By 15 min all measures except sensory thresholds had returned to baseline values. Thus, swallowing function is highly influenced by chemosensory input, providing insight into how oral sensation regulates pharyngeal swallowing.

Administration, Oral↗

Nitric oxide modulates elicitation of reflex swallowing from the pharynx in rats.

The pharynx is very important for elicitation of reflex swallowing. The region of the pharynx is innervated by the pharyngeal branch of the glossopharyngeal nerve (GPN-ph). Nitric oxide (NO) plays an important role in various physiological functions. The purpose of this study is to investigate the contribution of NO to reflex swallowing evoked by electrical stimulation of the GPN-ph. Swallowing was evoked in urethane-anesthetized rats by application of repetitive electrical stimulation (10- to 20-microA amplitude, 10- to 20-Hz frequency, 1.0-ms duration) to the central cut end of the GPN-ph or superior laryngeal nerve. Swallowing was identified by electromyographic activity of the mylohyoid muscle. Latency to the first swallow and the interval between swallows were measured. Intravenous administration of N(G)-nitro-L-arginine (L-NNA, 0.6 mg/kg), a nonselective inhibitor of NO synthase (NOS), extremely prolonged latency to the first swallow and the interval between swallows evoked by the GPN-ph. Intraperitoneal administration of 7-nitroindazole (5.0 mg/kg), a selective inhibitor of neuronal NOS, significantly prolonged latency to the first swallow and the interval between swallows evoked by the GPN-ph. Administration of L-arginine (an NO donor, 500 mg/kg) and sodium nitroprusside (an NO releaser, 0.6 mg/kg) restored the suppression of swallowing induced by the NOS inhibitor. Superior laryngeal nerve-evoked swallowing was suppressed by administration of a higher dose of L-NNA (6.0 mg/kg). Swallowing evoked by water stimulation of the pharynx was also suppressed by L-NNA (0.6 mg/kg). These results suggest that NO plays an important role in signal processing for initiation of reflex swallowing from the pharynx.

Animals↗

The relationship between rhythmic swallowing and breathing during suckle feeding in term neonates.

Little is known of the development of efficient coordination between suckle feeding and breathing in human infants. To establish baseline data, we recorded breathing and swallowing activity during bottle feeds in 23 infants at 14-48 h postnatal age. Most swallows (overall mean 68%) were organized into runs, with intervals starting at 0.6-0.8 s and slowing to 1-1.3 s after 30-40 s. The proportion of run swallows to total swallows increased significantly with age. Swallow intervals were regular (coefficient of variation = 18-38%) compared with breathing (coefficient of variation = 50%). Both breathing rate and tidal volume were significantly reduced by the onset of suckle feeding, and the pattern of respiratory airflow became markedly irregular. Mild transient desaturation was common, but was not accompanied by changes in heart rate. Swallows could occur in all phases of breathing. Overall, equal numbers of swallows were preceded by expiration and inspiration, but twice as many were followed by expiration compared with inspiration. Swallows were classified by the respiratory phases both preceding and following the swallow. Swallows occurred in all possible classifications in each of the infants studied. The incidence of the most frequent classification (inspiration-swallow-expiration), was 24% overall (individual range 5-50%). The phase relation between swallows and breaths changed frequently but showed occasional short periods of stability during which the breathing became regular and tidal volume increased. We conclude that at less than 48 h the normal infant has little coordination between swallowing and breathing rhythms and maintains rhythmic swallowing at the expense of eupnea.

Bottle Feeding↗

Electrical stimulation for swallowing disorders caused by stroke.

BACKGROUND: An estimated 15 million adults in the United States are affected by dysphagia (difficulty swallowing). Severe dysphagia predisposes to medical complications such as aspiration pneumonia, bronchospasm, dehydration, malnutrition, and asphyxia. These can cause death or increased health care costs from increased severity of illness and prolonged length of stay. Existing modalities for treating dysphagia are generally ineffective, and at best it may take weeks to months to show improvement. One common conventional therapy, application of cold stimulus to the base of the anterior faucial arch, has been reported to be somewhat effective. We describe an alternative treatment consisting of transcutaneous electrical stimulation (ES) applied through electrodes placed on the neck. OBJECTIVE: Compare the effectiveness of ES treatment to thermal-tactile stimulation (TS) treatment in patients with dysphagia caused by stroke and assess the safety of the technique. METHODS: In this controlled study, stroke patients with swallowing disorder were alternately assigned to one of the two treatment groups (TS or ES). Entry criteria included a primary diagnosis of stroke and confirmation of swallowing disorder by modified barium swallow (MBS). TS consisted of touching the base of the anterior faucial arch with a metal probe chilled by immersion in ice. ES was administered with a modified hand-held battery-powered electrical stimulator connected to a pair of electrodes positioned on the neck. Daily treatments of TS or ES lasted 1 hour. Swallow function before and after the treatment regimen was scored from 0 (aspirates own saliva) to 6 (normal swallow) based on substances the patients could swallow during a modified barium swallow. Demographic data were compared with the test and Fisher exact test. Swallow scores were compared with the Mann-Whitney U test and Wilcoxon signed-rank test. RESULTS: The treatment groups were of similar age and gender (p > 0.27), co-morbid conditions (p = 0.0044), and initial swallow score (p = 0.74). Both treatment groups showed improvement in swallow score, but the final swallow scores were higher in the ES group (p > 0.0001). In addition, 98% of ES patients showed some improvement, whereas 27% of TS patients remained at initial swallow score and 11% got worse. These results are based on similar numbers of treatments (average of 5.5 for ES and 6.0 for TS, p = 0.36). CONCLUSIONS: ES appears to be a safe and effective treatment for dysphagia due to stroke and results in better swallow function than conventional TS treatment.

Aged↗

Relationship between swallow rate and salivary flow.

Recent studies indicate that swallow-induced, primary peristalsis is a major determinant of normal esophageal acid clearance. However, factors that regulate the rate of spontaneous swallowing in normal subjects are incompletely understood. We postulated that the rate of salivary flow influences the rate of spontaneous swallows. To test this hypothesis, we did a total of 60 studies measuring salivary flow or the rate of spontaneous swallowing in 10 healthy volunteers, age 10-30 years. Saliva was collected by expectoration. Swallow rate was recorded by a small, transnasal catheter stationed in the pharynx and also, in some circumstances, by cervical electrodes. On separate sessions, we evaluated the effect of five test manipulations on salivary flow and swallowing rate, respectively. The test manipulations consisted of: (1) pharyngeal intubation, (2) sucking of a dummy lozenge, (3) sucking of a peppermint lozenge, (4) bethanechol injection (5 mg subcutaneously), and atropine administration (12 micrograms/kg intravenously). Pharyngeal intubation caused a small, but significant increase in the rate of salivation and spontaneous swallows. Sucking of a peppermint lozenge caused a sixfold increase in salivary flow while nearly doubling the swallowing rate whereas the dummy lozenge caused only a modest increase in salivary flow and swallowing. Cholinergic stimulation by bethanechol elicited a substantial increase in salivary flow and swallowing rate. In contrast, atropine caused a significant decrease in both salivary flow and swallowing. We conclude that in awake, normal subjects the rate of spontaneous swallows is influenced directly by salivary flow. Because oral lozenges substantially increase both swallowing rate and salivary flow, such agents merit investigation as a potentially useful ancillary treatment for the relief of heartburn.

Adolescent↗

The search for the central swallowing pathway: the quest for clarity.

As the work of Dr. Martin Donner has brought a clarity to understanding swallowing, so has the work of various neuroscientists, including that of a Nobel Laureate, in providing us with a better comprehension of this complex motor pattern. Understanding the neural control of swallowing has been a process that has occurred during this century in which several investigators, primarily from Europe, Japan, Canada, and the United States, have brought their perspectives in applying particular techniques to decipher how the central and peripheral nervous system control swallowing. Swallowing represents a complex muscular response of the oral, pharyngeal, and esophageal regions which are integrated to provide an effective functional pattern that prepares and transports food while simultaneously protecting the airway. This adaptation of the upper gastrointestinal tract in mammals has been extensively studied peripherally by two methods: recording from the peripheral nerves and muscles, and stimulating peripheral nerves and their receptive fields that can induce the pharyngeal and esophageal phases of swallowing. The study of the peripheral nervous system has provided insight into the sensory receptive fields that evoke or facilitate swallowing, and has established the first serious evidence of the all-or-none sequential contraction pattern of the oropharyngeal and esophageal muscles. It has been these electromyographic studies of the muscles that has established much of the criteria for evaluating the central swallowing pathway. Five techniques have been applied to the central nervous system to study swallowing and include lesioning or destroying discrete regions to determine how swallowing is impaired or modified, electrically stimulating the central neural tissue to determine the type of effects on swallowing, recording from the central neural tissue with macro- and microelectrodes to ascertain when neurons respond in timing to the peripheral muscle activity during swallowing, applying pharmacological agents through micropipettes which could mimic or inhibit potential transmitters, and using immunochemical techniques to tag specific chemicals that could be transmitters used by the neurons in the central swallowing pathway. These various techniques have provided insight into how the central swallowing pathway is organized but the details of the central control are still in the process of being defined and will require as much effort this next century as has been previously developed over the past 90 years.

Brain Stem↗