Brain, Vol. 123, No. 9, 1863-1873,
September 2000
© 2000 Oxford University Press
Abnormal patterns of breathing during swallowing in neurological disorders
1 Department of Medicine (Neurology), University of Wales College of Medicine, Cardiff and 2 Department of Neurology, Royal United Hospital, Bath, UK
Correspondence to:
Dr S. Hadjikoutis, Department of Neurology, University Hospital of Wales, Heath Park, Cardiff CF14 4XN, UK E-mail: Hadjikoutissa{at}cf.ac.uk
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Abstract |
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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.
motor neurone disease; swallow apnoea; dysphagia; dysphagia; respiration
DRG = dorsal respiratory group; EDAT = Exeter Dysphagia Assessment Technique; FVC = forced vital capacity; MND = motor neurone disease; ND = patients with neurological disorders; NO = subjects without a history of swallowing, breathing or neurological disorders; NTS = nucleus tractus solitarius; VRG = ventral respiratory group; xE = swallow apnoea followed by expiration; xI = swallow apnoea followed by inspiration
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Introduction |
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In humans, the pharynx serves as a common pathway for both swallowing and breathing. This anatomical configuration allows the possibility of aspiration of material into the airway. Several mechanisms minimize the risk of laryngeal penetration and/or aspiration: swallowing results in reflex closure of the glottis which acts as a protective valve against the aspiration of foreign materials into the respiratory tract (Ardran et al., 1952). Strong adduction of the true vocal cords is supplemented by the closure of the false cords and approximation of the aryepiglottic folds, although adduction of the true cords alone suffices to prevent penetration into the trachea. The epiglottis contributes to deflection of the bolus away from the laryngeal aditus into the pyriform sinuses, from which it passes into the oesophagus. Swallowing must also interact with breathing so that a swallow causes minimal or no disturbance to continuous breathing. In awake human adults, studies have shown that swallow events are accompanied by an apnoeic period (the swallow apnoea) lasting between 0.6 and 2.0 s (Clark, 1920
; Preiksaitis et al., 1992), and this swallow apnoea is followed by expiration in 95% of swallows (Selley et al., 1989a). This sequence of a swallow followed by expiration may be a useful mechanism for clearing the pharyngeal recesses of foreign residues before subsequent inspiration and may have a role in preventing low-grade recurrent aspiration.
The swallowing centre is a complex organization of neural elements in the cortex and brainstem of the CNS. In sheep, the neurones in the brainstem that are involved in swallowing lie mainly in the dorsal region, in and adjacent to the nucleus tractus solitarius (NTS) and the ventral region around the nucleus ambiguus with extensive involvement of the reticular formation (Jean, 1972, 1978Jean, 1984 Jean, 1986). The two regions are represented on both sides of the brainstem and are extensively interconnected (Doty, 1968). However, whether this work on animals is also applicable to man is uncertain. Breathing is regulated from complex interactions between two functional groups of neurones in the medulla known as the dorsal (DRG) and ventral respiratory groups (VRG). The DRG is located in the dorsolateral portion of the nucleus of the solitary tract. It primarily receives inputs from the cranial nerves IX and X, and specifically from the carotid body. The DRG sends fibres to the inspiratory spinal motor neurones and to the VRG, which it modulates (Cohen et al., 1974). The VRG is split into two parts: the rostral portion, primarily part of nucleus ambiguus, innervates the larynx and has both inspiratory and expiratory functions. The larger caudal part, also known as the nucleus retroambiguus, has both inspira- tory and expiratory neurones innervating motor units of the diaphragm and intercostal muscles. The descending axons of neurones contained in the DRG and VRG descend in the ventrolateral columns of the spinal cord, anterior to the corticospinal tract. Both inspiratory and expiratory axons appear to descend in somewhat different parts of the ventral portion of the cord (Newsom-Davis et al., 1972). The shared vagal motor innervation of pharynx and larynx via nucleus ambiguus and the close anatomical relationship between respiratory and pharyngeal afferents [to potentially overlapping regions of the nucleus of the tractus solitarius as shown in experimental animals (cat) (Kalia et al., 1980)] and the medullary respiratory centres suggest the basis for the high level of coordination between breathing and swallowing, including the inhibition of breathing during swallow apnoea (Doty, 1967). Studies using magnetic brain stimulation in patients with cerebral hemisphere stroke (Hamdy et al., 1996) together with previous clinical observations of swallowing in patients with cerebral hemisphere lesions (Meadows, 1973) have confirmed the importance of corticobulbar connections in facilitating swallowing in the conscious state and provide evidence for the importance of oropharyngeal afferent stimulation (Hamdy et al., 1998). Magnetic stimulation techniques in patients with discrete magnetic resonance documented brainstem lesions have also clarified the lateralization and brainstem course of relevant pathways to the hypoglossal nucleus (Urban et al., 1996, 1997).
Dysphagia is a symptom that may occur for many reasons (Hughes et al., 1998): there may be impaired motor control or weakness of facial, masticatory, pharyngeal or laryngo-oesophageal muscles; oropharyngeal sensation which aids triggering of the swallow reflex and protection of the airway may be abnormal; the conscious level may be diminished, thus removing in whole or part, voluntary control over deglutition; or the cerebral cortex may be damaged. A disruption of the normal coordination of swallowing and breathing has been shown previously in a small group of dysphagic neurological patients (Selley et al., 1989b), but the extent of its clinical significance and whether specific lesions or disorders of particular pathways cause this breakdown remain unclear.
There are two main techniques for monitoring breathing during swallowing: direct airflow (oral, nasal, or both oral and nasal airflow being monitored) and measurements related to changes in inflation of the lung, focusing on movements of chest wall and abdomen (Tarrant et al., 1997). The aim of our study was to investigate what factors (neurological or otherwise) determine the direction of airflow (inspiration or expiration) immediately after a swallow: this requires a sensitive technique such as that described by Selley et al. in the Exeter Dysphagia Assessment Technique (EDAT) based on nasal airflow (Selley et al., 1989Selley et al., 1990). It has been shown that EDAT is a valid (Selley et al., 1994) and reliable technique (Pinnington et al., 2000) in assessing breathing pattern during swallowing. We further attempted to clarify whether, in a particular disorder [motor neurone disease (MND)], postdeglutition inspiration per se is clearly linked to events likely to affect prognosis. First, a cross-sectional study was designed, using patients with defined neurological disorders, involving various structures or pathways, in order to determine whether lesions at particular sites resulted in the breakdown of the normal breathing pattern around a swallow. This study was not restricted to patients who complained of swallowing problems or who had clinical dysphagia. Normal subjects were also assessed and their breathing/swallowing pattern was compared with that of neurological patients. Secondly, a longitudinal study was designed to assess the interaction of breathing and swallowing in patients with MND, whose features are predominantly the result of corticobulbar/corticospinal or brainstem/spinal motor neurone pathology, and commonly associated with swallowing difficulties. We wished to identify factors associated with an abnormal pattern (i.e. swallow apnoeas followed by inspiration) and to clarify whether such a pattern is in fact related to chest infections, episodes of coughing and choking during meals, and prognosis. If this were the case, there might be specific guidance and treatment which should be considered by the speech and language therapist. Preliminary data on neurological patients (Pickersgill et al., 1998) and MND patients (Hadjikoutis et al., 1999) have been presented at meetings of the Association of British Neurologists.
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Methods |
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Subjects
Patients with a variety of defined neurological disorders (ND) were recruited from the neurology ward and clinics at University Hospital of Wales, and the rehabilitation and spinal injury unit ward at Rookwood Hospital, from September 1996 to August 1998. ND patients were classified by an investigator blind to the swallowing–breathing pattern results according to the site (cerebral hemisphere, brainstem, cerebellum, spinal cord, peripheral nerves) and pathways involved in the lesions using the case notes and imaging documentation. None of the patients had a history of a primary lung disease. Table 1
summarizes the neurological diagnoses of the patients. Subjects without a history of swallowing, breathing or neurological disorders (NO) were also recruited from hospital staff and the general public. Patients with MND, diagnosed according to El Escorial criteria (El Escorial, 1998), were recruited from the neurology ward, the general neurology clinics at University Hospital of Wales and the MND clinic at Rookwood Hospital, from June 1998 to September 1999. One of the MND patients had a history of a primary lung disease (chronic obstructive airway disease). ND and NO subjects were studied on one occasion. MND patients were studied at 3 monthly intervals for 12–15 months. Figure 1 summarizes the design of the study.
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Techniques
Bulbar and respiratory assessment
A standard questionnaire on swallowing-related symptoms for which normative data is available (Hughes et al., 1996a) was administered and a detailed general neurological examination was performed where bulbar signs were documented using a semiquantitative scale (Hughes et al., 1996a) and were divided into upper motor neurone signs [presence of a brisk jaw jerk, slow moving tongue, pseudobulbar affect (sudden loss of emotional control, i.e. laughing, crying or both occuring in response to non-specific, often inconsequential stimuli in the absence of clear association with prevailing mood state)] and lower motor neurone signs (tongue wasting, fasciculations, weakness, palatal/pharyngeal muscle weakness, absent gag reflex, uvula deviation, hoarseness of voice). However, we appreciated that in some severe cases of bulbar weakness, a definite distinction of lower and upper motor neurone weakness was difficult. A quantitative measure of swallowing capacity was obtained by a test in which the time and number of swallows required to consume a known volume of water was measured: average volume per swallow (ml), average time per swallow (s) and swallowing capacity (ml/s) were calculated (Hughes et al., 1996b). An abnormal test of swallowing was defined as being a swallowing capacity or volume/swallow less than the lower 95% confidence interval for the individual predicted mean adjusted for age and sex. Eating habits (diet modification and feeding assistance) were documented. Respiratory function was assessed by recording forced vital capacity (FVC) using a portable spirometer (a face mask was used in patients with bulbofacial involvement).
Breathing pattern during swallowing
The breathing pattern during swallowing was recorded using intranasal pressure measurement (Selley et al., 1990). This method employed nasal speculae inserted into the nostrils and relied upon the reduction of pressure within the nares on inspiration and conversely, a slight increase in pressure above atmospheric on expiration due to the flowing air. By connecting the speculae to a sensitive micromanometer within the EDAT device (Bio-instrumentation Ltd, Exeter, UK) the pressure changes can be detected. Entry of a bolus into the mouth was recorded by completion of an electrical contact made with an insulated plastic cup. Swallow sounds were recorded via a throat microphone held below the angle of the mandible or lateral to the thyroid cartilage, and distinguished from artefact by using an electronic marker when elevation of the larynx was observed and swallow sounds heard via headphones. Signals from the EDAT equipment were presented in chart form using a Gould Electronics TA240 EasyGraf four channel chart recorder. The optimum chart speed for subsequent analysis of respiratory and swallow events was 10 mm/s. Subjects were asked to swallow boluses of tepid tap water presented in the plastic cup at volumes of 5, 10 and 20 ml. Eight swallows of each bolus volume were recorded for ND and NO subjects, with the exception of patients with significant dysphagia whose average volume per swallow during the timed test of swallowing dictated that boluses should be restricted to 5 or 10 ml for reasons of safety. ND and NO subjects were also asked to perform eight `dry' swallows, i.e. no bolus being presented to them, merely to initiate a voluntary swallow. The 32 swallows were performed in random order. Between three and six boluses of each volume (5, 10 and 20 ml) were given to MND patients randomly. For each swallow, the following were recorded: (i) the number of swallows per bolus swallow; (ii) the length of each swallow apnoea; (iii) the pattern of breathing after each swallow apnoea; (iv) respiratory rate before each swallow.
Each swallow apnoea was classified into one of two types depending on whether it was followed by expiration (xE) or inspiration (xI). Figure 2 illustrates an example of an xE swallow and measurements taken from the chart recording. The proportion of xI swallows in the individual patients with neurological disorders was compared with the grouped proportion in normal subjects. Pearson correlations and one-way analyses of variance or the Kruskal–Wallis test were used to investigate relationships between the proportion of each swallow type, and the clinical and respiratory measurements taken, both within and between the two groups.
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MND patients were classified into two groups according to whether they did or did not have xI swallow apnoeas and the two groups were compared for certain prospectively defined demographic, disease related, bulbar related, respiratory related or prognostic variables. Nineteen out of 32 MND patients had a repeat assessment after an interval of 6 months (range 6–9 months). The remaining 13 patients were unable to have a second assessement: seven had died, two were unable to swallow orally, and four were unable to cooperate due to severe disability.
Coughing/choking episodes, chest infections, prognosis
MND patients used a pre-formatted sheet to maintain a detailed diary of coughing and choking events together with any association with eating and drinking over 3 days close to the day of the assessment. Patients were asked to report any chest infections during the follow-up period. The following criteria were used in defining a chest infection: fever, coughing, discoloured sputum, prescription of antibiotics for a chest infection by the general practitioner or hospital doctor. Medical notes of all patients were checked for any possible admissions in local hospitals with chest infections. Patients were assessed every 3 months for up to 15 months duration in order to record coughing and choking episodes, chest infections and prognosis. The duration of the disease from the onset of MND symptoms until the end of the study or death was recorded. Deaths were recorded via listing with the Office of Population and Census Surveys and copies of death certificates were obtained.
Ethics
The study was approved by Bro Taf Local Research Ethics Committee in Cardiff. All patients and healthy volunteers gave consent for the study.
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Results |
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Patients with defined neurological disorders (ND) and normal subjects (NO)
Twenty-two healthy volunteers [13 female, mean age 49 (range 21–73) years] were assessed. A total of 484 swallows were analysed. Twenty out of 22 (91%) individuals always displayed a swallow apnoea followed by expiration (xE) regardless of bolus size (5–20 ml); 2/22 (9%) displayed an xI swallow pattern, and this occurred only with a 20 ml bolus in 50% of swallows.
Twenty-two patients [18 male, mean age 49 (range 21–76) years] were studied, 662 water boluses were presented (5, 10, 20 ml) and 965 swallows occurred, associated with 1023 apnoeas; of these a mean of 18.9% (range in individual patients 2.8–70.6% of all swallows) in 20/22 (91%) patients were followed by inspiration (Table 1
). Two patients had no xI swallows. There was a significant difference between the two groups (healthy volunteers and neurological patients) in the proportion of swallow apnoeas followed by inspiration (xI swallows) (P < 0.001, Kruskal–Wallis test).
Six patients had abnormal swallowing as defined by the quantitative swallowing test (Table 1) of whom four complained of swallowing symptoms. These six patients had significantly more xI swallows (P < 0.02, one-way analysis of variance) than those with a normal timed test of swallowing. Sex, age, forced vital capacity and respiratory rate before each swallow were not associated with the frequency of xI swallows.
Patients were divided into three groups according to the anatomical site of their neurological disorder: brain (group 1), spinal cord (group 2) and peripheral nervous system (group 3) (Table 2). Patients with brain and peripheral nervous system disease tended to have a lower swallowing capacity in terms of volume/time and volume/swallow than patients with spinal cord disease: this pertained whether absolute values were used (Table 2) or if results were expressed in relation to normal values for age and sex. Patients with spinal cord injury or disease tended to have a lower FVC than patients with brain or peripheral nervous system disease. xI swallows were not associated with any specific anatomical site of neurological disease (Table 2). Patients were also classified according to neurological pathways likely to be impaired: patients with corticobulbar involvement (four patients) had more (%) xI swallows (mean = 38.9%, SD = 22.9) than those without (mean = 15.8%, SD = 20.2), but the diference was not statistically significant (P = 0.15, Kruskal–Wallis test).
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MND patients
Frequency of xI swallows
Thirty-two MND patients [22 male, mean age 67 (range 51–81) years] were studied (Table 3
). Fourteen patients (44%) had at least one swallow apnoea followed by inspiration (xI patients) at the initial assessment: six patients had an xI swallow with 5 ml bolus, seven with 10 ml bolus, and 10 with 20 ml bolus (Table 4). In 18 (56%) patients, apnoea was always followed by expiration (xE patients). Figure 3 illustrates an example of a patient with an xI swallow.
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Factors related to xI swallows
xI patients were more likely to have upper motor neurone bulbar signs and had a much lower swallowing capacity both in terms of volume/time and average volume/swallow than xE patients (Table 3
). Age, sex, duration of the disease, respiratory rate and FVC were not associated with an abnormal respiratory pattern during swallowing (Table 3). Patients with xI swallows generally had longer swallow apnoeas (Table 4) and required more swallows to clear a bolus compared with those with xE swallows: this was significant for 20 ml (using the Kruskal–Wallis test, P < 0.023 and P < 0.002, respectively) but not 5 and 10 ml boluses. Figure 4 illustrates an example of a patient with prolonged swallow apnoea and multiple swallows with a 20 ml bolus.
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Follow-up assessments
Two out of 19 MND patients who had repeat studies of swallowing–breathing pattern developed an xI swallow at the second examination (with a 5 ml bolus), nine continued to display only xE swallows, and eight continued to display at least one xI swallow. The two patients who developed an xI swallow pattern during the follow-up (group 1) had a lower swallowing capacity and longer duration of apnoea than the patients who continued to display xE swallow (group 2) (Table 5
); one required percutaneous endoscopic gastrostomy (PEG) and nocturnal assisted ventilation by nasal mask.
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Clinical significance of xI swallows
Four patients had had chest infections since the diagnosis of MND; two of those always had xE swallows, whereas two sometimes had xI swallows (25–33% of swallows for 20 ml bolus). Fifteen out of 32 patients recorded episodes of coughing and choking during meals during the 3 days close to the day of the assessment. The number of coughing and choking episodes was not associated with an abnormal breathing pattern during swallowing (Table 3
). Seven out of 32 patients died during the 18 months follow-up of whom two had had an abnormal respiratory pattern during swallowing (Table 3). |
Discussion |
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The coordination of respiration and swallowing in healthy volunteers and patients with defined neurological disorders has been studied. The study confirmed that the great majority of swallow apnoeas in normal awake adults are followed by expiration (Nishino et al., 1985
; Selley et al., 1989a). However, in a variety of neurological disorders and lesion sites, the swallow apnoea is followed by inspiration more frequently than expected. This might increase the risk of aspiration or laryngeal penetration. It might be expected that the motor neurone activity in the nucleus ambiguus innervating pharyngeal and laryngeal muscles is functionally linked to activation of respiratory motor neurones. Lesions in the region of the nucleus of the tractus solitarius, or more generally in the medulla oblongata might be anticipated to cause more disruption of this link than simple respiratory or pharyngeal/laryngeal muscle weakness due to spinal or peripheral neuromuscular diseases. However, the study indicates that an abnormal respiratory pattern during swallowing (xI swallows) can occur in a purely spinal disorder or in a purely peripheral neuromuscular disorder affecting breathing or swallowing: indeed CNS (including brainstem) pathology was no more likely to cause disruption than peripheral pathology. In particular, a patient with selective peripheral involvement of inspiratory muscles (patient 19) due to phrenic nerve palsies had a marked tendency to postdeglutition inspiration. One patient (11) with intact inspiratory function but severe impairment of expiratory muscle function had no xI swallows whilst others with lower cervical cord lesions and thus impairment of expiratory muscle function had an increased incidence of such xI swallows. Respiratory muscle dysfunction with normal swallowing may thus be associated with disruption of the normal pattern in the absence of any clinical suggestion of brainstem impairment. A patient with no neurological lesion but mechanical tethering of the tongue (22) and a modest reduction in swallowing capacity had xI swallows on almost 25% of attempts. Such findings suggest that direct neural involvement of swallowing related pathways is not necessary for xI swallows to occur and, conversely, that intact swallowing and brainstem function does not necessarily prevent postdeglutition inspiration, whatever its cause. This suggests that breakdown of the normal pattern may be the result of disorded swallowing or breathing in some individuals rather than the two problems having common cause. Possible explanations for this may include a respiratory override if the swallow apnoea is long or multiple swallows are required to clear a bolus (e.g. Fig. 4).
A significant proportion (44%) of MND patients displayed post-apnoea inspiration after a swallow: there may be several reasons for this. Reduced swallowing capacity (caused by reduced volume/swallow and/or increased time/swallow), prolonged swallow apnoeas and increased number of swallows to clear large boluses (20 ml) are significantly associated with xI swallows. The two patients who initially had a normal respiratory pattern during swallowing but developed an xI swallow pattern during follow-up had also developed a significant decline in their swallowing capacity. It seems possible that the automatic respiratory control system prevails over the swallowing reflexes when the maintenance of ventilation is particularly important in conditions of loaded breathing, since the time available for breathing could be significantly reduced by repeated swallows and prolonged swallow apnoeas. Furthermore, many patients with MND probably develop type II respiratory failure due to denervation of the respiratory muscles. Hypercapnia influences the co-ordination of breathing and reflex swallowing by increasing the frequency of inspiration immediately after the swallow apnoea (Nishino et al., 1998). One may suppose that, even though a reduced FVC was not associated with xI swallows in this study, at a critical point during the development of respiratory failure, very prolonged swallow apnoeas and raised PaCO2 contribute to make an xI swallow more likely. A serial study with measurement of oxygen saturation and PaCO2 might be required to investigate this further. One of the limitations of this study is that we have not used non-volitional respiratory tests. Volitional control of respiration can be impaired by corticospinal tract lesions (Howard et al., 1992), as may occur in MND, and therefore FVC measurements give an incomplete picture of respiratory function in these patients.
The cross-sectional study has shown that the specific nature and location of the neurological lesion does not seem to be closely associated with changes in the respiratory pattern during swallowing. However, patients with corticobulbar involvement tended to display greater percentage xI swallow than those without. The longitudinal study in patients with MND has clearly shown that patients with upper motor neurone bulbar signs had significantly more xI swallows than those without. Loss of corticobulbar fibres may weaken descending inhibition of inspiration during swallow apnoea and increase the likelihood of an inspiration event triggered by the automatic respiratory system following a swallow.
It has been suggested that the coupling of swallows with expiration may be one of several mechanisms by which the airway is protected from aspiration during swallowing (Smith, 1989). Therefore it could be anticipated that post deglutition inspiration might contribute to the risk of aspiration or laryngeal penetration so that more episodes of coughing and choking might be expected. However, abnormal respiratory pattern during swallowing was unrelated to chest infections, episodes of coughing and choking during meals and prognosis. Although we have not systematically used videofluoroscopy to assess silent aspiration in these patients, the low frequency of clinical respiratory events makes it unlikely that any aspiration was major or clinically significant. Recent studies support the view that other factors apart from mechanical aspiration should be considered in the pathogenesis of aspiration pneumonia: these include oral/dental status, host resistance, pulmonary clearance and smoking (Langmore, 1998). Furthermore, it is also important to emphasize that the pattern of breathing after a swallow as assessed by a water bolus may not necessarily be the same as that associated with other types of bolus (e.g. solid or semisolid food, or thickened fluids) (Preiksaitis et al., 1996). It is evident from Table 3 that some MND patients were already on a modified diet at the time of the assessment so that the respiratory pattern recorded during the test procedure might not be fully representative of that during normal life at home (e.g. some patients avoided water).
In conclusion, the swallow apnoea in patients with brain, spinal cord and peripheral neurological lesions is followed by inspiration more frequently than expected. This seems to occur irrespective of the site of the lesion(s). MND patients commonly display an abnormal respiratory pattern during swallowing characterized by: inspiration after swallow, prolonged swallow apnoea and multiple swallows per bolus, but this was unrelated to chest infections, coughing and choking episodes during meals and prognosis. It seems likely that postdeglutition apnoea inspiration is more important as an indicator of disordered swallowing or breathing rather than being an important mechanism of aspiration per se or of symptom production.
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Acknowledgments |
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The authors are also grateful to R. E. Ellis and F. C. Flack at the Department of Medical Physics, University of Exeter for their invaluable help regarding EDAT equipment and measurements (further details regarding EDAT equipment can be acquired from R. E. Ellis, Medical Physics Group, Department of Physics, University of Exeter, Stocker Road, Exeter EX4 4QL, UK). We are also grateful to the consultants in Neurology and Rehabilitation for permitting study of patients under their care. S.H. is supported by a bequest for MND research and a Grant from Schering AG. T.P.P.'s research was funded by Schering AG. EDAT equipment was funded by Action Research.
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Received January 10, 2000. Revised April 10, 2000. Accepted May 22, 2000.
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