| Abstract|| |
Swallowing transiently increases heart rate. One of the authors developed pronounced bradycardia while breath holding, particularly after an expiration. The objective, therefore, was to study his cardiac responses during swallowing as pronounced bradycardia developed. When, after a maximum inspiration (supine), the heart rate slowly fell below 50 beats min' well-defined P waves (lead II) disappeared. By swallowing 6 times on command after the P waves disappeared his heart rate increased immediately (68 ± I beats min-'; n=6). P waves with similar morphology to those pre-swallowing were recorded 0.7 ± 0.1 s (n=6) after the first swallow. He continued breath holding after swallowing. P waves again disappeared, although at faster heart rates (57 ± I beats min'; n=6). Furthermore, well-defined P waves were observed after the second disappearance at heart rates within the range 30-40 beats min'. Small amplitude P waves continued to be recorded from lead I with P wave disappearance in lead II, suggesting a pacemaker shift, although not to the av node. Autonomic nerves can shift the dominant pacemaker within the sa node. The present report indicates that increased vagal tone may be rapidly reversed by swallowing.
|How to cite this article:|
Ballal MA, Sanford PA. Swallowing-induced cardio-respiratory responses in man. Saudi J Gastroenterol 1998;4:81-9
The swallowing process and respiration are intimately related  . Thus when man swallows breathing is inhibited, usually in the inspiratory position (deglutition apnea). Both swallowing and respiration are accompanied by changes in heart rate. Transient tachycardia occurs while swallowing  and the sinus arrhythmia of breathing has long been established  . Most investigations of these relationships have involved the use of anesthetized animals. However, cardiovascular and respiratory events are notoriously sensitive to anesthetic agents  . Human studies, using alert volunteers, offer an important means of avoiding some of the pitfalls of anesthetized animal experiments. The present report is of such a study. One of the authors (P.A.S) developed pronounced bradycardia when breath holding , . It was found that when his heart rate fell slowly below 50 beats min -1 his P wave flattened and disappeared. Usually P wave disappearance is regarded as a pathophysiological event with the av node assuming a dominant pacemaker role. However, this subject had no history of cardiovascular problems so that a unique opportunity was available to study the mechanisms involved in the disappearance of P waves under physiological conditions and to investigate the influence of swallowing on these events.
| Methods|| |
The subject was one of the authors (P.A.S., [Table - 1]). He had no history of cardiovascular problems. After preliminary experiments (i) he provided 24 hours ECG records using a Holter monitor, and (ii) he underwent and successfully completed a cardiac stress test using the Bruce protocol in the Clinical Physiology Unit at King Khalid University Hospital. No cardiac abnormalities were detected. He was asked to hold his breath under a variety of conditions, usually (but not always - see procedure (j)) until he reached his breaking point. In some experiments he was instructed to swallow at specific times whilst breath holding. In others he was asked not to swallow voluntarily and to record those occasions on which the stimulus could not be ignored and he was obliged to swallow. He held his breath while:
(a) prone, after a maximum expiration with the face immersed in water at 4° C,
(b) prone, after a maximum expiration with the face immersed in water at 4° C, and swallowing every 5 seconds (s),
(c) sitting quietly after a maximum inspiration,
(d) sitting quietly after a maximum inspiration, and swallowing every 5 s after 60 s of breath holding,
(e) prone, after a maximum inspiration,
(f) prone, after a maximum inspiration with the face immersed in water at 4° C,
(g) prone, after a maximum inspiration with the face immersed in water at 4° C, having breathed 100% oxygen for the 20 s before breath holding,
(h) supine, after a maximum inspiration,
(i) supine, after a maximum inspiration, and swallowing 6 times in rapid succession when instructed after the P wave had disappeared,
(j) supine, after a maximum inspiration, and swallowing 6 times in rapid succession when instructed, having breathed 100% oxygen for the 20 s before breath holding. The command to swallow was given after 90 s breath holding. A continuous ECG record was obtained using a Siemen's Cardiostat 701 (lead 11) or Litton's Multiscriptor EK 26 (leads I, II and III). This included a 60 s resting period before any experimental procedure was followed, the breath holding period itself and a 60 s recovery period after the breaking point had been reached. The heart rate was determined from the mean R-R interval of 5 s recordings and expressed as beats min -1 . Maximum R-R intervals were also noted and expressed in s. Significant differences were determined using the Student test. To facilitate swallowing the flow of saliva was increased with a Smith and Kendon Original Travel Sweet (acid lemon flavor), Terry's Group, York, held bucally. ECG data from a number of experiments was collected with the Biopac System (Biopac System Inc., Santa Barbara, CA 93117). A conventional ECG trace was simultaneously taken. Using the Biopac System a respiration transducer (Pneumotrace) could be wrapped around the neck to monitor swallowing and compare this event with cardiac electrical changes.
| Results|| |
When the subject was asked to immerse his face in water after a maximum expiration in the prone position, his breath holding time was 27.7 ± 0.9 s (n=7). However, when he swallowed at 5 s intervals after face immersion his breath holding time was significantly increased to 41.4 ± 0.9 s (n=7; p<0.001; [Table - 2]). Changes in R-R interval occurring during breath holding after a maximum expiration with the face immersed in water while swallowing and not swallowing are shown in [Figure l]a. If not swallowing the R-R interval smoothly increased as the subject held his breath. However, if he swallowed every 5 s the R-R interval transiently decreased so that the pronounced bradycardia developed more slowly [Figure - 2]a.
a) Swallowing and breath holding times
When the subject was asked to hold his breath without voluntarily swallowing after a maximum inspiration in the sitting position his breaking point was reached in 93.4 ± 1.4 s (n=17; [Table - 2]). If after 60 s, he was encouraged to swallow every 5 s his breath holding time was increased to 116.3 ± 1.7 s (n=7; p<0.001). His heart rate, as shown by changes in R-R interval, was transiently increased with each swallow [Figure l]b and pronounced bradycardia during breath holding developed less rapidly [Figure - 2]b.
(b) P wave disappearance
As the heart rate of the subject fell slowly below 50 beats mini' the P wave of the ECG flattened and disappeared [Table - 3], and reappeared only, but immediately after the breaking point was reached [Figure - 3]. This was found whether breath holding after a maximum inspiration: (i) in air while in either the prone or supine position, the breaking point being achieved at a later time in the latter (p<0.001).
(ii) with the face immersed in water at 4° C after or without breathing 100% oxygen for 20 s. Oxygen breathing resulted in a less pronounced bradycardia. Thus the heart rate fell only marginally below 50 beats min -1 , the maximum R-R interval recorded being 1.26 ± 0.03 s (n=6). Nevertheless, P waves disappeared after 122.7 ± 2.4 s (n=6), almost a minute before the breaking point was reached. ECGs recorded using lead I gave P waves which were of small amplitude, making any changes associated with breath holding difficult to recognize.
(c) Swallowing and P wave disappearance:
[Table - 4] shows the results obtained when the subject held his breath after a maximum inspiration in the supine position and swallowed 6 times on command as the P wave disappeared. As in earlier experiments the P wave disappeared when the heart rate fell below 50 beats min -1 . However, P waves with pre-disappearance morphology were recorded in 0.74 ± 0.13 s (n=6) after starting to swallow and were maintained during the swallowing period (9.4 ± 0.2 s; n=6; [Figure - 4]). The heart rate during the swallowing period was remarkably constant [Table - 5].
The subject continued breath holding after his 6 swallows. The P wave disappeared a second time. The heart rate at which it disappeared, however, was more rapid than that at the first disappearance (57.2 ± 0.9 c.f. 50.5 ± 1.0 beats min -1 ; n=6; p<0.001; see [Table - 4]). Furthermore, well-defined P waves were recorded at heart rates considerably slower than 50 beats min -1 in contrast to the continued absence of P waves when non-swallowing protocols were followed.
Results are also included in [Table - 5] of experiments in which 6 swallows were taken after breathing 100% oxygen and breath holding for 90 s. Under these conditions the heart rate had not fallen when compared with the pre-breath holding rate. An increase of 10 ± 1 beats min -1 (n=6) was observed during the swallowing period.
| Discussion|| |
In this study swallowing has been shown to be associated with two distinct but interrelated physiological events. One is the breath holding time, the other the electrical changes recorded with every heart beat.
The increased breath holding time following either a maximum expiration or maximum inspiration when the subject swallowed is in agreement with the observations made by Comroe (1965)  . When breath holding after a maximum expiration the subject was in the prone position with his face immersed in water at 4°C. He swallowed every 5 s while breath holding. This frequency was chosen as it is readily tolerated. Furthermore, Meyer, Gerhard and Castell (1981)  have shown that when paired swallows are separated by a 5 s interval the amplitude of the initial peristaltic wave is depressed while that of the subsequent swallow is normal. These observations point to the effectiveness of later swallows. Swallowing while breath holding after a maximum expiration was conducted with the face immersed in water to ensure that room air was not taken into the mouth with each swallow. A different problem arose with experiments involving a maximum inspiration. In these the subject was asked not to swallow for the first 60 s of his breath holding time, but subsequently to do so at every 5 s. To swallow in every 5 s for more than 100 seconds proved difficult. Furthermore, pronounced bradycardia did not develop within the first minute in these experiments [Figure - 2]b.
The heart rate during swallowing was found to increase transiently. Tachycardia in response to swallowing has been described  . It is difficult to explain how swallowing might produce this response. A clue may be provided by the well established changes associated with the respiratory cycle (sinus arrhythmia) and the finding that many of the medullary neurones firing at the start of inspiration are also activated during swallowing .
Numerous posssible explanations might be suggested for the increase in breath holding times observed when swallowing. Comroe (1965)  commented that swallowing appeared to depress the respiratory centre. An alternative view might be that the transient tachycardia alters the perfusion pattern of peripheral chemoreceptors, thus reducing their afferent discharge and contribution to the distress of breath holding. Certainly the bradycardia of breath holding developed more slowly when the subject swallowed [Figure - 2].
Several other factors may contribute to the increase in breath holding times recorded when swallowing. For example, by concentrating on swallowing man may be distracted from ever increasing distressful stimuli. In addition, by causing upper respiratory tract movements swallowing may centrally remove a distress-related input. In the same way that swallowing may prolong breath holding times so respiratory movements have been proposed to be of major importance in distracting the vigorously exercising athlete from chemical stimuli which might have been expected to cause considerable distress 
The basic question that needs to be addressed is why man is forced to breathe and why swallowing might delay the breaking point. Both chemical and non-chemical factors must contribute. Models have been developed by Godfrey and Campbell (1969)  and Courteix, Bedu, Fellmann, Heraud and Coudert (1993)  to explain the interrelationships of these different factors. In these models the absence of respiratory movements produces signals which induce the accumulation of a central excitatory state (CES) in a pool of respiratory neurones. When chemical factors and the CES act together on the respiratory "centre" the respiratory muscles are stimulated. However, during breath holding respiratory muscles do not effectively shorten although muscle tension increases. The resulting discharge from muscle, tendon or joint receptors produces unpleasant sensations. Swallowing and respiratory movements may remove the CES and some of the urgency to breath.
An examination of the ECG has shown that as the heart rate slowly falls below 50 beats min -1 the P wave flattens and disappears, albeit at very different times depending on the protocols employed. Abnormal P waves have previously been recorded during breath holding if the faces of volunteers were immersed in water  . Such abnormalities were never recorded while breath holding in air. The present observations confirm those of Whayne and Killip (1967)  . They described P wave disappearance during simulated diving. They interpreted their findings in terms of the physiological pacemaker being shifted to a lower centre (the av node). In all but one instance the nodal rhythm generated was during face immersion. The one exception involved a subject whose face was covered by a wetted cloth at 0° C. In the present study the P wave disappeared while breath holding either in air or with the face immersed provided the heart rate fell slowly. This may reflect the more pronounced bradycardia of this subject while breath holding in air. Convincing changes in P wave morphology after a maximum expiration have not been recorded in the present study. The more precipitous declines in heart rate accompanying such breath holding protocols may result in the heart virtually stopping before any alteration of pacemaker activity can occur.
The observation that P waves, admittedly of small amplitude, could be recorded from lead I when the well-defined P waves from lead II had flattened and disappeared indicated that the av node had not become the dominant pacemaker. Other explanations of P wave disappearance need to be looked for. One possibility is that atrial muscle and the sa node may be differentially affected by the vagus  with the result that the sa node continues to pace ventricular contractions in the absence of atrial contractions. A more likely explanation is that the site of the dominant pacemaker cells in the sa node is altered. The heterogeneity of sa node cells has been established both in terms of the cells' morphology  and the receptors they contain  . Both branches of the autonomic nervous system have been shown to shift the pacemaker, the vagus caudally and the sympathetic nervous system rostrally , . As the heart slows under the greater influence of the vagus nerve the shift of pacemaker could result in atrial electrical activity originating at, and being distributed from a different focus thus altering the signal recorded from conventional surface leads.
The present study clearly shows that the P wave can be restored rapidly in lead II, usually within one cardiac cycle of the first swallow. The returning P waves had a similar morphology to those recorded before swallowing. The P waves were maintained throughout the swallowing time during which the heart accelerated. However, when the swallowing protocol had been completed and the subject continued breath holding, the heart rate again started to slow and the P waves again disappeared although at heart rates significantly faster than those at which the P wave first disappeared. The pacemaker may have shifted at an earlier stage. The instability of the system is further indicated by the finding that P waves of pre-swallowing morphology could be recorded when the heart fell below 40 beats min -1 , an occurrence that was not seen when the P waves disappeared during non-swallowing experiments. If the dominant sa node pacemaker cells can be changed so quickly by swallowing there would seem to be a readily available means by which excessive vagal tone could be voluntarily but transiently reduced.
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Paul Anthony Sanford
Department of Physiology, College of Medicine, King Saud University, P.O. Box 2925, Riyadh 11461
Source of Support: None, Conflict of Interest: None
[Figure - 1], [Figure - 2], [Figure - 3], [Figure - 4]
[Table - 1], [Table - 2], [Table - 3], [Table - 4], [Table - 5]