Voluntary and Reflex Influences on the Initiation of ... - Springer Link

Dysphagia 16:40–47 (2001) DOI: 10.1007/s004550000041 © Springer-Verlag New York Inc. 2001

Voluntary and Reflex Influences on the Initiation of Swallowing Reflex in Man Cumhur Ertekin, MD,1 Nefati Kiylioglu, MD,1 Sultan Tarlaci, MD,1 A. Bulent Turman, MD,2 Yaprak Secil, MD,1 and Ibrahim Aydogdu, MD1 1

Departments of Neurology and Clinical Neurophysiology, Ege University, Medical School Hospital, Bornova, Izmir, Turkey, 2Department of Biomedical Sciences, University of Sydney, Sydney, New South Wales, Australia

Abstract. The electrophysiological features of voluntarily induced and reflexive/spontaneous swallows were investigated. In normal subjects, swallows were elicited by infusing water either into the mouth (1–3 ml) or directly into the oropharyngeal region through a nasopharyngeal cannula (0.3–1 ml). For water infused orally, subjects were either requested to swallow voluntarily or instructed to resist swallowing and maintain the horizontal head position until swallowing occurred reflexively. Spontaneous saliva swallowing was investigated in patients with severe dysphagia who had a prominent clinical picture of suprabulbar palsy. Comparisons between different swallowing types were made by measuring the time interval between the onset of submental electromyographic activity (SM-EMG) and the onset of the upward movement of the larynx recorded by a movement sensor. This interval was less than 100 ms, even frequently less than 50 ms, in reflexive/spontaneous swallows, while in voluntarily induced swallows it was substantially longer. The rising time of submental muscle’s excitation was also shorter in reflexive/spontaneous swallows. It was suggested that the triggering of voluntarily induced swallows commences more than 100 ms before the onset of swallowing reflex and that this mechanism is under the control of corticobulbar– pyramidal pathways. If the swallowing reflex is triggered within such a short period of time following the onset of SM-EMG, the central control by the bulbar swallowing center should be effective until the end of oropharyngeal swallowing.

Presented at the 9th European Congress of Clinical Neurophysiology Ljublujana, 1998, and 11th International Congress of EMG and Clinical Neurophysiology Prague, 1999. Correspondence to: Prof. Dr. C. Ertekin, Nilhan Apt. 1357 sok. No-1 D-10 Alsancak, I˙zmir, Turkey. E-mail: [email protected]

Key words: Deglutition — Triggering of swallow — Neurophysiology of reflex swallow — Deglutition disorders.

There is a close relationship between voluntary attempts to swallow and triggering of the pharyngeal phase of the swallowing reflex. During orophyaryngeal swallowing, the oral phase begins with the contraction of the striated submental (SM) muscle complex located on the floor of the mouth [1–4]. The contraction of SM muscles pulls up the hyoid bone into an anterosuperior position which elevates the larynx and initiates other reflex changes that constitute the pharyngeal phase of swallowing [1,2,5]. Movements that occur from the beginning of SM muscle contraction to the elevation of the larynx are important for safe passage of the bolus to the pharyngoesophageal segment without escaping into the other cavities. The contraction of SM muscles continues until the completion of the oropharyngeal swallowing process [2,3,6–9]. Therefore, when a swallow is initiated voluntarily, the contraction of these muscles should be controlled by at least two routes. During the initial phase, SM muscles should be activated by means of corticobulbar– pyramidal drive to the bulbar swallowing center. The latter phase, however, should be controlled mainly by reflex mechanisms arising from the bulbar center itself, particularly the period immediately after the onset of laryngeal upward movement, which is an important and early event of the swallowing reflex [1,10]. Therefore, overall, the voluntarily initiated swallow consists of two components: the initial voluntarily induced neuromuscular activity that positions the bolus in the oral cavity and the following pharyngeal response which is controlled by a reflex swallowing mechanism. However, the voluntary

C. Ertekin et al.: Electrophysiology of Swallowing

and reflex phases of swallowing have not yet been studied in detail by means of electrophysiological methods and their mechanisms are not clearly understood. In this study we investigated the electrophysiological properties and the linkage between different phases of voluntarily and involuntarily initiated swallows. It has been possible to analyze the phases of swallowing with the electrophysiological method described. Materials and Methods The electrophysiological methods used for the evaluation of oropharyngeal swallowing were described previously [6,8,11]. Briefly, a mechanical sensor that consists of a single piezoelectric wafer, with a rubber bulge affixed at its center, was place over the coniotomy region between the cricoid and thyroid cartilages on the midline. The sensor was secured with a rubberband tied around the neck and its output was connected to one of the channels of the EMG apparatus (Medelec Mystro, MS 20, Surrey, England; cutoff frequencies at 0.01–20 Hz). During each swallow the sensor gave two deflections of generally opposing polarity. To time-lock all the signals to the same event, one of the edges of the first deflection was used to trigger the delay-line circuitry of the recording apparatus. The first deflection recorded by the laryngeal sensor coincided with the upward movement of the larynx and the onset of the second deflection began with the onset of the laryngeal downward movement. The time interval between the onsets of two deflections was referred to as the 0–2 time interval and corresponded to the total relocation time of the larynx during oropharyngeal swallowing [6,12]. The upward and downward deflections of the laryngeal sensor were sometimes diphasic or triphasic for technical reasons. Their shortest time with high amplitude at the beginning of the deflection from the baseline was important; this was measured from superimposed and averaged traces of five swallows for each condition. The shape of the second deflection of the laryngeal sensor was partly deformed during averaging process because of the swallowing jitter [6,8,12], but the onset point of second deflection could be measured by both averaged and superimposed traces of swallows. The EMG activity was recorded using bipolar silver chloride EEG electrodes taped under the chin over the mylohyoid–geniohyoid– anterior digastric muscle complex (referred to as the submental EMG or SM-EMG). The EMG signals were bandpass filtered (between 100 Hz and 10 kHz), amplified, rectified, integrated, and then averaged. As these muscles are laryngeal elevators, their activity gave information about the onset and duration of swallowing [2,3]. The preanalysis time was set at 800 ms and the total sweep duration was 2 or 5 s. At least five successive sensor and SM-EMG signals were recorded simultaneously for each swallowing condition. The signal traces collected were examined individually and in superimposed and averaged form. A total of 16 healthy subjects and 17 patients (Table 1) participated in the study. In each healthy subject, the voluntarily induced swallows were investigated first. The subject was seated and instructed to hold his/her head in the natural upright position. For each swallowing maneuver, 1–3 ml of tap water was placed in the mouth midway between the tip and base of the tongue via a fine syringe. When the water was in position and the tip of the tongue was touching the upper incisors, the subject was asked to swallow following the examiner’s swallow command [13]. During this process, the SM-EMG and laryngeal biomechanical activity were recorded. The swallowing pattern was closely followed on the oscilloscope screen; an incomplete or inappropriate swallow was excluded from the study [6,7]. Spontaneous or reflexive swallows were obtained in association with various conditions outlined below.

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Reflexive Swallows During investigation of healthy participants, the subject was instructed to recline on an examination table with the head on a headrest at an angle of about 30° from the horizontal plane. For each swallow, 1 ml of tap water was introduced to the back of the tongue with a syringe. The subject was instructed not to make any effort to swallow the water voluntarily but to maintain the head position with the month open until the water was swallowed reflexively. In our study, this kind of swallowing was called reflexive. It was previously shown [14] that spontaneous swallows can be obtained with the mouth and head in this position. Reflexive swallows were obtained from 16 healthy volunteers (mean age ⳱ 28.5 years, range ⳱ 19–42 years, 11 males and 5 females). For each subject, reflexive swallowing was repeated several times prior to initiation of recording procedures. Reflexive swallows were also compared with the subjects’ voluntarily induced swallows.

Nasopharyngeal Swallows In eight subjects (mean age ⳱ 31.1 years, range ⳱ 19–42 years, 5 males and 3 females), the swallowing pattern was investigated using the nasopharyngeal swallowing method. In this technique, swallowing was induced by water presented through a plactic catheter or cannula (outer diameter ⳱ 3 mm). The cannula was inserted into one of the nostrils and down into the uvula level of nasopharyngeal space (about 7 cm from the nostril to the nasopharynx). To avoid the triggering of gag reflex, precaution was taken so that the plastic cannula did not advance beyond the level of soft palate and uvula. While the subject’s head was in a slightly hyperextended position, 0.3–1 ml of water was dripped through the cannula. Because of the subglottic aspiration or gag reflex, usually no more than 1 ml could be tolerated. The results of nasopharyngeal swallows were compared with voluntarily induced swallows.

Spontaneous Saliva Swallows (SSS) Spontaneous saliva swallows were obtained from neurological patients with severe dysphagia. A total of 17 patients were investigated for their swallowing functions (Table 1). Eleven patients had had a stroke or suprabulbar palsy (SBP) resulting from vascular insults; six had had motor neuron disease (ALS) with prominent suprabulbar signs. Although spontaneous saliva swallows could be obtained from all patients studied, voluntarily induced swallows could not be recorded in 7 patients who were being fed through nonoral routes since they could not swallow voluntarily. In the remaining 10 patients, there was some difficulty in triggering the oropharyngeal swallows; however, it was still possible to compare the electrophysiological patterns of voluntarily induced swallows with spontaneous saliva swallows. Usually, 1–3 ml of water could safely be swallowed voluntarily, and accumulation of saliva in the mouth easily triggered the spontaneous swallows. Our study was performed according to the ethical priniciples of the Declaration of Helsinki (1964) concerning human experimentation and approved by the Ethics committee of our University Hospital. Informed consent was obtained from each subject. The Student t test was used to look for the differences between the groups of subjects. A value of p < 0.05 (two-sided) was considered a significant difference. Data are presented as the mean ± standard error of mean.

Results Comparison of Reflexive Swallows with Voluntarily Induced Swallows The data obtained from 16 healthy subjects during reflexive swallowing were analyzed and compared with

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Table 1. Summary of the clinical findings of patients investigated

No.

Patient

Age

Gender

Etiological diagnosis

Suprabulbar palsy

Clinical dysphagia

Nonoral feeding

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

A.K. H.C. K.C. A.K. A.A. S.H. M.A. C.D. M.G. F.S. E.U. M.B. B.S. T.G. Y.A. M.K. S.M.K.

62 65 60 62 42 58 41 57 71 74 49 52 65 55 74 68 77

Male Male Male Male Male Female Male Male Male Female Female Male Male Male Male Male Male

ALSa ALS ALS ALS ALS ALS Strokeb Stroke PBPc PBP PBP PBP PBP PBP PBP PBP PBP

+ + + + + + + + + + + + + + + + +

+ + + + + + + + + + + + + + + + +

+ – – + – – – – – – + + + + – – +

a

ALS; motor neuron disease was diagnosed according to the El Escorial criteria [32]. Bilateral sequential large infarcts were diagnosed according to MRI and clinical findings. c Multiple lacunar infarcts were diagnosed according to the MRI and clinical findings. b

data collected during voluntarily induced swallowing. Interval and amplitude parameters related to these swallowing types are shown in Table 2. A representative electrophysiological recording is illustrated in Figure 1. The most significant difference between these two swallowing types was the time interval between the onset of SM-EMG and the onset of upward deflection of the larynx [7,8]. This time interval—referred as the A–0 interval—was significantly shorter for reflexive swallows than for voluntarily induced swallows (p < 0.05). Similarly, the rising time for the recruitment of SM-EMG was also shorter in reflexive swallowing (p < 0.05). Overall, the total duration of SM-EMG (A–C interval) was shorter for reflexive swallows (p < 0.05). However, the latter part of the SM-EMG activity, measured from the onset of laryngeal upward deflection (0) to the end of SM-EMG (C), (i.e., 0–C interval), did not differ significantly during voluntarily induced and reflexive swallows (p > 0.05). Furthermore, the laryngeal relocation time (0–2 time interval) and the peak amplitude of SM-EMG were not significantly different during these two types of swallowing. Analysis of EMG recordings from individual subjects, as seen in Figure 1, revealed that, in all subjects studied, the A–0 time interval of reflexive swallows was < 100 ms (even ⱕ 50 ms in 10 out of 16 subjects). However, during voluntarily induced swallows, the same interval was never 0.05

55.5 ± 6 24 10–148 69 ± 4.8 19.4 27–104 > 0.05

784.6 ± 60.7 242.9 346–1200 735.7 ± 36.2 144.9 486–1062 > 0.05

a

Mean ± SEM–SD–Range. Time between the onset of SM-EMG (A) and the onset of upward deflection of larynx (0). c Time from the onset to the negative peak of SM-EMG. d Total duration of SM-EMG. b

Fig. 1. Recordings of voluntary and reflexive swallows obtained from a normal subject. Top Laryngeal movement obtained by the sensor. Bottom Integrated SM-EMG. Both the A–0 time intervals (arrows) and the rising time of SM-EMG (hatched area) were shorter in reflexive swallows. The laryngeal relocation times (0–2 interval) were not different. Five swallows are averaged for each trace. SM-EMG is submental EMG, 0–2 interval is the laryngeal relocation time, A–C interval is the duration of submental EMG activity.

without difficulty. Measurements of various parameters of SSS (17 patients) and voluntarily induced swallows (10 patients) are shown in Table 4. Figure 5 shows the voluntarily induced and SSS recordings from a dysphagic patient with suprabulbar palsy. In all 10 patients from whom voluntarily induced swallows could be obtained, the A–0 time interval was significantly shorter (mean ⳱ 17 ± 2.8 ms, range ⳱ 2–36 ms) during SSS compared with voluntary swallows (p < 0.05). Furthermore, the total duration of SM-EMG (A–C interval) and the rising time of SM-EMG were also comparatively shorter (p < 0.05 for both parameters), and the mean amplitude of SM-EMG was smaller (p < 0.05) during SSS. However, it should be noted that the laryngeal re-

e

Time between the onset of two laryngeal deflections (laryngeal relocation time). f Amplitude from baseline to negative peak. g Time from the onset of upward deflection (0) to the end of the SMEMG (C).

Fig. 2. Comparison of A–0 intervals during voluntarily induced (VIS) and reflexive swallows (RS) obtained from 16 normal subjects. The individual A–0 interval values of all reflexive swallows (squares) are < 100 ms and mostly accumulated around 50 ms. However, voluntarily induced swallows (triangles) never commence within 100 ms before the initiation of the reflex phase of swallowing. SM-EMG is submental EMG, 0–2 interval is the laryngeal relocation time, A–C interval is the duration of submental EMG activity.

location time (0–2 time interval) was found to be similar for both SSS and voluntarily induced swallows. The significant increase in the total duration of SM-EMG during voluntarily induced swallowing in these patients must be related to the abnormal prolongation of the A–0 time interval that is associated with the delay in triggering the swallowing reflex (Fig. 5). The latter part of SM-EMG duration that follows the onset of upward movement of the larynx was not prolonged in voluntarily induced swallows. Figure 6 shows the A–0 time intervals of voluntarily induced, reflexive, and nasopharyngeal swallows

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Fig. 3. Comparison of voluntarily induced and nasopharyngeal swallows obtained from a normal subject. During nasopharyngeal swallowing both the A–0 intervals (arrows) and the rising time of SM-EMG (hatched area) were shorter compared with voluntarily induced swallows. The laryngeal relocation times (0–2 interval) were similar. Five swallows are averaged in each trace. 0–2 interval is the laryngeal relocation time, A–C interval is the duration of submental EMG activity.

obtained from normal subjects and the same intervals of spontaneous saliva swallows obtained from the patient group. It was observed that the A–0 time interval was shortest in SSS of the patient group and that this interval increased possibly as a result of lesser sensitivity of the other swallowing conditions studied. Nevertheless, it can be proposed that the duration of the genuine reflex phase of a swallow, measured from the onset of SM-EMG (or the onset of swallowing) to the onset of reflex upward movement of larynx (the onset of reflex swallowing), should be about 50 ms or less. On the other hand, the laryngeal relocation time (0–2 time interval), which demonstrates the pharyngeal phase of swallowing reflex, never changed significantly in any of the swallowing conditions, including the voluntarily induced swallows (p > 0.05). This was also the case for the latter half of SM-EMG duration that followed the onset of the laryngeal upward movement (p > 0.05).

Discussion The major finding of this study was the importance of the relationship of the time between the onset of submental muscle activation and the onset of the laryngeal upward movement for identification of voluntary and reflex phases of the voluntarily induced swallows. This time parameter, denoted as the A–0 interval, is closely linked with the triggering of the reflex phase of swallowing or the pharyngeal response. The A–0 time interval was found to be >100 ms (range 160–418 ms) in all voluntarily induced swallows, while it was always 0.05

a

Mean ± SEM–SD–Range. Time between the onset of SM-EMG (A) and the onset of upward deflection of larynx (0). c Time from the onset to the negative peak of SM-EMG. d Total duration of SM-EMG. b

Fig. 4. The effect of water volume on swallowing patterns during nasopharyngeal swallowing. If the water volume is > 1 ml, a normal subject divides the bolus into two pieces (piecemeal deglutition). Each trace is a single recording. Each line beneath SM-EMG traces denotes one swallow. SM-EMG is the duration of submental EMG activity.

reflex phase is directly triggered during spontaneous swallows. Such a brief triggering time and brisk responsiveness may indicate that the fast afferent route and rapid control of the reflex mechanism involve the bulbar center. The functional organization of this neural circuit may be related to the protective nature of spontaneous swallows [26]. One may speculate that voluntarily induced swallows are triggered at the junction of the oral and pharyngeal cavities, while spontaneous swallows, such as in sleep, are triggered from the pharyngeal cavities. Indeed, the swallows obtained by the nasopharyngeal cannula support this argument and indicate that reflex swallows are triggered immediately after dropping water into the pharynx, since the entrance to oropharynx was bypassed by the nasopharyngeal cannula. However,

e

Time between the onset of two laryngeal deflections (laryngeal relocation time). f Amplitude from baseline to negative peak. g Time from the onset of upward deflection (0) to the end of the SMEMG (C).

it was also apparent that the pharyngeal cavities are very sensitive to even very small bolus volumes and can produce double or multiple swallows. Therefore, the initial site for piecemeal deglutition or repetitive swallows for one bolus [12,13] is the pharyngeal cavities rather than the oral cavity. Although during voluntarily induced swallows the triggering mechanism of the swallow is possibly initiated from the oral space, an unexpected escape of small pieces of the bolus into the pharyngeal space should initiate secondary reflex swallows. Spontaneous saliva swallowing should also be triggered from the pharyngeal region. Although the entire pattern of oropharyngeal swallowing can be experimentally elicited by cortical stimulation of the frontal cortical center and the corticobulbar pathway [27–31], there is no direct evidence that suggests the cortex is able to elicit a complete oropharyngeal swallowing in man. The evidence for the importance of corticobulbar control over the first part of SM-EMG comes from both healthy subjects and patients with clinical involvement of the corticobulbar system. In normal subjects, during voluntarily induced swallows the A–0 interval was considerably long (艌100 ms). In some patients with corticobulbar involvement, although voluntary attempts to swallow had disappeared, spontaneous swallows were still functional. However, in these patients the triggering time for the reflex phase of swallowing, i.e., the A–0 interval, was 0.05

a

f

b

g

Mean ± SEM–SD–Range. Time between the onset of SM-EMG (A) and the onset of upward deflection of larynx (0). c Time from the onset to the negative peak of SM-EMG. d Total duration of SM-EMG. e Time between the onset of two laryngeal deflections (laryngeal relocation time).

Fig. 5. Recordings of voluntarily induced and reflexive swallows obtained from a dysphagic patient with suprabulbar palsy. During reflexive saliva swallows, typically both the A–0 time intervals (arrows) and the rising time for SM-EMG (hatched area) were very short. During voluntarily induced 3-ml water swallows, the triggering of the swallowing reflex (A–0 interval) was delayed and produced a longer SM excitation period (A–C interval). The laryngeal relocation time (0–2 interval) of the reflex phase of swallowing was almost the same in both types of swallowing. 0–2 interval is the laryngeal relocation time, A–C interval is the duration of submental EMG activity.

Amplitude from baseline to negative peak. Time from the onset of upward deflection (0) to the end of the SMEMG (C). h SSS-spontaneous saliva swallows; obtained from 17 patients. i VIS-voluntarily induced swallows; obtained from 10 patients.

Fig. 6. Comparison of A–0 intervals of various swallowing types obtained from normal subjects and patients. From the patients, reflexive swallows (n ⳱ 17) were obtained, and from normal subjects, nasopharyngeal (n ⳱ 8), reflexive (n ⳱ 16), and voluntarily induced (n ⳱ 16) swallows were obtained. The measurements calculated and plotted for each group are shown on the explanatory bar.

ing may have access to a common interneuronal pool in the bulbar center [30]. Nevertheless, it appears that at least the spontaneous “saliva” swallowing is predominantly controlled by the central pattern generator of the bulbar swallowing center in response to the urge to swallow the saliva accumulation in the oropharyngeal cavities [3,23]. Acknowledgement. This work was supported by a grant from the Turkish Scientific and Technological Research Council (TUBITAK) (Project No. SBAG- 1739).

Fig. 7. Schematic of neural pathways operating during voluntarily induced and reflexive swallows.


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