Journal of Oral Rehabilitation 2006 33; 402–408
Effect of reclining and chin-tuck position on the coordination between respiration and swallowing T . A Y U S E * , T . A Y U S E †, S . I S H I T O B I * , S . K U R A T A †, E . S A K A M O T O †, I . O K A Y A S U † & K . O I † *Department of Special Care Dentistry, Nagasaki University Hospital of Medicine and Dentistry and †Department of Translational Medical Sciences, Course of Medical and Dental Sciences, Division of Clinical Physiology, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki, Japan
Chin-tuck position and reclining posture have been used in dysphagia patients to prevent aspiration during swallowing. However, both behavioural treatments may affect respiratory function. This study was carried out to test the hypothesis that if chin-tuck posture and body reclining affected respiratory function, this would be associated with altered coordination between respiration and swallowing. To investigate this hypothesis, respiratory parameters and manometry were used in each of four combinations of reclining posture and chintuck position. In the 60 °reclining with 60 °chintuck position, duration of swallowing apnea (0Æ89 SUMMARY
Introduction The swallowing reflex is a complex reflex that involves coordinated contraction of several muscles in the mouth and upper airway, including the pharynx. Therefore, mandible and body-neck positions may affect the functional controls of swallowing. Although several experimental evidences support the clinical observation of neuro-physiological, structural and functional interdependence between the upper airway system and swallowing function (1–6), a high degree of coordination between respiration and swallowing is essential for the maintenance of adequate ventilation without causing pulmonary aspiration. In dysphagia patients, swallowing exercises in the reclining position (7, 8) and chin-tuck position (9, 10) have been effective in eliminating aspiration during swallowing. Nevertheless, it has been suggested that excessive application of these manoeuvres may cause a major influence in the ª 2006 Blackwell Publishing Ltd
s.d. 0Æ17 s) and submental electromyography burst (2Æ34 s.d. 0Æ84 s) were significantly longer when compared to both upright sitting and 30 °reclining positions. We conclude that 60 °reclining from vertical with 60 °chin-tuck may affect oral processing stages which delay and reduce a variety of oropharyngeal movements. These in turn significantly influence the coordination between respiration and swallowing. KEYWORDS: chin-tuck position, swallowing apnea, manometry, respiratory function Accepted for publication 4 October 2005
respiratory function, including upper airway patency (11, 12), and reduction of laryngeal elevation. Palmer et al. (13–15) highlighted the importance of oral processing from the end of Stage I (transport of ingested material from the incisal area to the molar region of the oral cavity) until the initiation of Stage II (movement of triturated food from the oral cavity through the pillars of the fauces to the oropharyngeal surface of the tongue). To complete this sequence of the oral processing stages that include taking food into the mouth, chewing the food to reduce particle size, mixing the food with saliva, and placing the food between the tongue and hard palate in a ‘ready to swallow’ position, the position of tongue and occlusal plane is a critical issue. We hypothesized that a combination of chin-tuck position and reclining posture may have significant influence on the coordination between respiration and swallowing. To date, no studies have examined this doi: 10.1111/j.1365-2842.2005.01586.x
COORDINATION BETWEEN RESPIRATION AND SWALLOWING Manometry sensor
Nasal mask
Poro
Pneumotacho 3cm
b Polyethylene tube 3cm
Phypo Pues
Submental EMG
Fig. 1. Diagram of the experimental set-up.
possibility. The purpose of this study was therefore to describe the effects of the reclining posture and chintuck position on the coordination between respiration and swallowing.
Materials and methods Subjects Ten healthy male subjects aged between 22 and 24 years (mean 23Æ2; s.d. 1Æ0 years) were studied. Subjects were of average built, and none had a history of dysphagia, gastrointestinal, neurological, or upper airway and pulmonary disease. All subjects provided written informed consent, and the ethics committee of Nagasaki University approved the study protocol. Figure 1 illustrates the experimental set-up. We performed submental electromyography (EMG) by placing a surface electrode 1 cm posterior to the genu of the mandible over the midline suprahyoid muscle complex. This signal was differentially amplified (Bioamp CF*) relative to a surface recording over the left zygomatic arch. An electrode over the right zygomatic arch served as the ground lead. The EMG signal was also whole-wave rectified, and integrated in 50 ms intervals. A three-sensor pressure transducer catheter (Gaeltec CTO-4†) was passed via the nares into the upper airway and esophagus to simultaneously measure upper esophageal sphincter pressure (Pues), hypopharyngeal pressure (Phypo) and oropharyngeal pressure (Poro). The proximal end of the catheter was inserted into a *AD Instruments, Sydney, Australia. † Dunvegan, Isle of Skye, Scotland.
sealed chamber and calibrated with a mercury manometer. Topical anesthesia was not used. The distances between the esophageal end of the catheter and the above-mentioned sensors were 18, 21 and 24 cm, respectively; consistent with those reported in a recent study (2). The sensors, which had surfaces covered with silicone membrane, were positioned with the transducers facing posteriorly. The catheter’s position was adjusted to obtain characteristic pressure recordings at the level of the oropharynx, hypopharynx and upper esophageal sphincter; when the most distal transducer was correctly positioned in the upper esophageal sphincter, a characteristic M-shaped configuration of the manometry wave appeared during swallowing. Once correct placement was achieved, the catheter was secured in position by taping it to the nasal bridge and the cheek. Airflow and nasal pressure (Pn) were monitored with a pneumotachometer (model 3830‡) and differential pressure transducer (model 1100‡). The dead space of this system was 150 ml. The airflow signal was filtered (low pass 100 Hz) and amplified, and zero flow was calibrated by removing the pneumotachograph from the mask. To calibrate volume, 3 L of air was passed through the pneumotachograph. All measurements were displayed and stored simultaneously on a desktop computer using Power lab data acquisition software (model 8sp*) and were also recorded on an eightchannel thermal recorder.
Experimental protocol The coordination between respiration and swallowing was examined in four different combinations of torso position and chin-tuck, with the occlusal plane kept parallel to the floor (Fig. 2): Condition I, upright sitting posture (0 reclining from vertical) with 0 chin-tuck (neutral position); Condition II, 30 reclining from vertical with 30 chin-tuck; Condition III, 45 reclining from vertical with 45 chin-tuck; Condition IV) 60 reclining from vertical with 60 chin-tuck. In each case, the subjects’ head was supported on a wedgeshape pillow. The subjects swallowed the injected water volitionally after holding it in the mouth. Swallowing was induced at a random point relative to the respiratory cycle, without warning the subjects, by administra‡
ª 2006 Blackwell Publishing Ltd, Journal of Oral Rehabilitation 33; 402–408
Hans Rudolph, Inc., Kansas City, MO, USA.
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T . A Y U S E et al. Experimental protocol
Condition II
Condition I
0°
Condition IV
Condition III
30°chin-tuck
0°chin-tuck
60° chin-tuck
45°chin-tuck
30°
45°
Fig. 2. Experimental protocol. The head is supported on custommade pillows (30 , 45 , 60 ) when subject is put in the reclining position with chin-tuck.
60°
Occlusal plane parallel to floor
deglutition apnea, which was determined from the EMG and airflow tracings. Swallows preceded and followed by inspiratory flow were classified as inspiratory swallows (I), whereas those preceded and followed by expiratory flow were designated expiratory swallows (E). Swallows occurring at the transition between inspiration and expiration were designated inspiratory–expiratory (IE) transition swallows, and those occurring at the transition between expiration and the inspiratory phase of the next breath were designated expiratory–inspiratory (EI) transition swallows.
tion of a bolus injection of 5 ml distilled water using a flexible polyethylene tube placed on the retromolar gingiva (Fig. 1). In each test condition, 10 boluses of water were administered at intervals of five breaths.
Data analysis Swallowing apnea time was assessed by measuring the plateau phase on the respiratory trace (nasal flow) (Fig. 3). The onset of swallowing was defined as the onset of the submental EMG burst and
Vnasal(mL s–1)
80 40 0 –40 –80
Phypo(mmHg) Pueso(mmHg)
800 400 0 –400 –800
EMG(uv)
Analysis of swallowing trace
Poro(mmHg)
404
80 40 0 –40 –80 80 40 0 –40 –80
Inhalation Peak hight
Submental EMG
Mean hight
Pre-swallow EMG
Duration
Upper esophageal sphincter
Hypopharynx
80 40 0 –40 –80
Swallowing apnea
2s
Duration apnea peak
Peak hight
Oropharynx 3:30
3:40
3:50
Fig. 3. Representative recording of the swallowing reflex. Swallowing was induced every four to five breaths. Upper inspiratory airflow (VI) (top channel), submental EMG activity (second channel from top), and manometry were performed to determine pressure at the upper esophagus (Peso), hypopharynx (Phypo) and oropharynx (Poro). The catheter’s position was adjusted to obtain characteristic pressure recordings at the level of the oropharynx, hypopharynx and upper esophagus. When the most distal transducer was correctly positioned in the upper esophagus, a characteristic M-shaped configuration of the manometry wave appeared during swallowing. ª 2006 Blackwell Publishing Ltd, Journal of Oral Rehabilitation 33; 402–408
COORDINATION BETWEEN RESPIRATION AND SWALLOWING The mean value of submental EMG activity in the pre-swallow level and the peak value of submental EMG activity during swallowing were characterized as follows. The mean s.d. for the digitized rectified EMG was calculated during the resting state for the digastric muscle; then, individual bursts were identified as readings of ‡ mean + 3 s.d. for more than 30 ms. Manometric analysis Manometry was performed at the upper esophageal sphincter (Pues), hypopharyngeal (Phypo), and oropharyngeal (Poro) levels. All manometric measurements were calculated as the mean of the 10 consecutive swallows. Upper esophageal sphincter (UES) resting tone (mmHg) was measured before the 10 swallows. Pressure recordings made at the level of upper esophageal sphinchter (Pues), hypopharynx (Phypo) and oropharynx (Poro) were analysed to determine contraction peak amplitude (mmHg) and duration of contraction (s). Resting pressure (mmHg), peak and lowest relaxed pressure (mmHg) were also obtained for the upper esophageal sphincter.
Statistical analysis Effects of reclining and chin-tuck position for each outcome variable were studied using ANOVA for repeated measures with post hoc Bonferroni adjustment (Kaleida, Graph 3Æ6). Because the data with small group of subjects may not be normally distributed, the results were cross-checked with Kruskal–Wallis one way ANOVA, a non-parametric test. The non-parametric analysis yielded essentially identical statistical findings. The
timing of swallowing in relation to the respiratory cycle was analysed by the Kruskal–Wallis test. P < 0Æ05 was considered significant. All the values are reported as mean s.d.
Results Table 1 shows analysis of transition between swallowing phases. No significant differences in tidal volume, respiratory rate or duration of respiratory cycle in the resting phase before swallowing were apparent between each position. In Condition IV, deglutition apnea time (0Æ89 s.d. 0Æ17 s) and submental EMG burst duration (2Æ34 s.d. 0Æ84 s) were significantly longer compared to both Conditions I and II (P < 0Æ05). In Condition IV, mean pre-swallow EMG activity (35Æ1 s.d. 10Æ5 lV) was significantly larger compared to both Conditions I and II. The period from onset of apnea to peak hypopharyngeal pressure (0Æ71 s.d. 0Æ19 s) and to peak EMG burst (0Æ29 s.d. 0Æ31 s) were also significantly longer in Condition IV compared to both Conditions I and II. Table 2 shows all manometric measurements for Pues, Poro and Phypo. In Condition IV, P which is lowest and indicates relaxed upper esophageal sphincter pressure (2Æ91 s.d. 4Æ16 mmHg) was significantly higher compared to that in Condition I (0Æ98 s.d. 3Æ43 mmHg). Table 3 shows timing of swallow in relation to respiratory cycle phase. Timing of swallowing did not differ significantly among the positions assessed.
Discussion The major finding in this study about the influence of reclining posture and chin-tuck position on the
Table 1. Analysis of transition between swallowing phases. Condition I Tidal volume (ml) Respiratory rate (breath min)1) Peak EMG activity (lV) Mean pre-swallow EMG activity (lV) Respiratory cycle duration (s) Swallowing apnea (s) EMG burst duration (s) Onset apnea – peak Poro (s) Onset apnea – peak Phypo (s) Onset apnea – peak Pues (s) Onset apnea – peak EMG burst (s) One way
ANOVA
585 16Æ3 135Æ8 10Æ4 3Æ72 0Æ78 1Æ45 0Æ39 0Æ58 0Æ59 0Æ03
63 4Æ2 55Æ8 5Æ3 0Æ12 0Æ19 0Æ75 0Æ14 0Æ18 0Æ18 0Æ07
Condition II 557 15Æ5 131Æ5 12Æ9 3Æ75 0Æ79 1Æ52 0Æ42 0Æ60 0Æ61 0Æ02
45 2Æ5 32Æ6 4Æ9 0Æ15 0Æ14 0Æ65 0Æ12 0Æ13 0Æ18 0Æ09
+ Bonferroni post hoc: *P < 0Æ05 vs Condition I; †P < 0Æ05 vs Condition II.
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Condition III 526 15Æ9 129Æ5 25Æ8 3Æ82 0Æ82 1Æ80 0Æ41 0Æ62 0Æ58 0Æ15
73 2Æ8 35Æ9 6Æ9 0Æ10 0Æ13 0Æ53 0Æ09 0Æ14 0Æ15 0Æ12
Condition IV 510 16Æ8 131Æ6 35Æ1 3Æ96 0Æ89 2Æ34 0Æ45 0Æ71 0Æ68 0Æ29
60 3Æ8 41Æ8 10Æ5*† 0Æ16 0Æ17*† 0Æ84*† 0Æ11 0Æ1 9*† 0Æ18 0Æ31*†
405
406
T . A Y U S E et al. Table 2. Manometric measurements for Pues, Poro, Phypo
Peak Poro (mmHg) Peak Phypo (mmHg) Presting Pues (mmHg) Plowest Pues (mmHg) Ppeak Pues (mmHg) One way
ANOVA
Condition 1
Condtion II
Condition III
Condition IV
91Æ91 19Æ03 77Æ73 27Æ55 21Æ17 5Æ69 0Æ98 3Æ43 85Æ37 10Æ55
92Æ03 16Æ14 79Æ86 22Æ69 20Æ37 6Æ52 1Æ73 3Æ39 86Æ36 7Æ30
90Æ06 19Æ81 71Æ5 25Æ8 22Æ74 6Æ78 1Æ39 3Æ62 80Æ86 14Æ46
89Æ80 19Æ34 78Æ09 24Æ20 25Æ93 6Æ43 2Æ91 4Æ16* 74Æ80 10Æ56
+ Bonferroni post hoc: *P < 0Æ05 vs Condition I.
Table 3. Timing of swallowing in relation to respiratory cycle phases Condition 1 Condition II Condition III Condition IV E type (%) IE type (%) EI type (%) I type (%)
85Æ1 9Æ8 4Æ2 1Æ1
92Æ8 4Æ2 2Æ0 1Æ5
97Æ1 1Æ9 0Æ0 1Æ0
94Æ3 2Æ7 1Æ0 2Æ0
coordination between respiration and swallowing in normal young subjects was that the durations of swallowing apnea and submental EMG activity were prolonged in 60 reclining from vertical with 60 chintuck position (Condition IV).
Swallowing apnea Recently, Olsson et al. (16) described laryngeal elevation as the single most important factor for a successful pharyngeal swallowing sequence. The major purpose of laryngeal elevation for respiratory function is thought to be airway closure during swallowing, i.e. deglutition apnea. The duration of swallowing apnea has been measured in several studies and mean duration appears to be between 0Æ6 s and 0Æ76 s in young subjects (17– 19) and 1Æ06 s in older subjects (20). Duration of swallowing apnea obtained in the upright sitting (Condition I) position (0Æ78 s.d. 0Æ19 s) in this study was therefore consistent with these previous data. In our study there appeared to be an increase in the duration of swallowing apnea from 0Æ78 s to 0Æ89 s with 60 reclining and 60 chin-tuck posture (Condition IV). A similar trend toward increasing apnea duration was also found by Perlman et al. (18) in younger subjects with increasing bolus volume. Possible mechanisms causing prolongation of apnea with increasing bolus volume have previously been discussed by Ertekin et al. (21), who concluded this phenomenon to be related to increased duration of submental EMG activity, UES
opening and laryngeal displacement. Recently Hiss et al. (22) suggested that swallowing apnea may occur secondary to a specific neural command from the brainstem but may also be a habituated motor response. We speculate that prolonged submental EMG activity and laryngeal displacement might affect neural command or motor response.
Submental EMG activity and manometric analysis It has been suggested that the EMG activity of the submental muscle complex (mylohyoid, geniohyoid and anterior digastric muscles) is closely related to that of laryngeal elevator muscles (23). Therefore, surface EMG activity of the submental muscle gives a considerable amount of information about the onset and duration of the oropharyngeal swallowing, because the contraction of the submental muscles pulls up the hyoid bone into an anterosuperior position, which elevates the larynx and initiates other reflexive changes that constitute the pharyngeal phase of swallowing. We observed that duration of EMG activity was significantly prolonged in Condition IV. Therefore, we speculate that this positional change affecting the oral processing stages may in turn delay the onset and reduce some movements in oropharyngeal swallowing as described above. Furthermore, we must consider the pre-swallow level of myoelectric activity. When a subject is in the position of 60 reclining from vertical with 60 chin-tuck position (Condition IV), the neck flexion is produced by strong contraction of the anterior neck muscles. This may include contraction of the anterior suprahyoid and infrahyoid muscles which are critically important for swallowing. In this study, we observed significant increase of pre-swallow mean submental EMG activity in Condition IV indicating higher tonic muscle activity before swallowing. Therefore, it may be difficult to initiate a swallow when these muscles are actively contracting to maintain neck flexion.
ª 2006 Blackwell Publishing Ltd, Journal of Oral Rehabilitation 33; 402–408
COORDINATION BETWEEN RESPIRATION AND SWALLOWING Manometric analysis provided supportive findings regarding the effect of reclining and chin-tuck position. We observed significant increases in time from onset of apnea to peak hypopharyngeal pressure, and time from onset to peak EMG burst in Condition IV. These results also indicate that the 60 reclining with 60 chin-tuck position (Condition IV) may cause a delayed onset of swallowing on oropharyngeal swallowing in earlier stages, i.e. oral processing stages between Stage I and Stage II.
Clinical implications We conclude that, if we keep the occlusal plane parallel to the floor, excessive chin-tuck might affect the coordination between swallowing and respiratory movements. We cannot infer that this lack of coordination is critical in dysphagia patients because this study was performed in normal young healthy subjects. However, it can be speculated that these changes of coordination between respiration and swallowing might be potentiated in patients with upper airway dysfunction (24) or respiratory disease (6, 25). A study by Shaker et al. (26) demonstrated that during disease exacerbations, patients with COPD swallow more often during the inspiratory than during the expiratory phase of the respiratory cycle. Teramoto et al. (24) suggested that patients with obstructive sleep apnea syndrome are likely to exhibit impaired swallowing, probably due to perturbed neural and muscular function of the upper airways. Although a simple extrapolation of the results of our study to other clinical situations may not be entirely valid, further studies are definitely needed to determine the most effective behavioural treatment for deglutitive aspiration in obstructive respiratory dysfunction.
is also difficult to know whether the observed differences in the 60 chin-tuck position are due to the trunk position, the neck position or both, since neither was assessed in the absence of the other. Nevertheless, the present results support the premise that it is possible to keep the occlusal plane parallel to floor in order to keep food and liquid in mouth during certain phases of swallowing. Second, we did not perform simultaneous video-radiographic form of imaging in this study. It is difficult to know what is happening during the period of delay from the time of onset of swallow apnea until the manometric and myoelectric events. Although simultaneous video-radiography and manometric assessment would enable further investigation of the mechanisms coordinating swallowing and respiration, we decided not to use the former technique in order to eliminate risks associated with radiation for normal subjects. Third, we used 5 ml of distilled water for initiation of swallowing so that the subjects swallowed volitionally after holding it in the mouth; further studies are needed regarding solid food swallowing. In conclusion, 60 reclining from vertical with 60 chin-tuck may affect oral processing stages which delay and reduce a variety of oropharyngeal movements.
Acknowledgments This study was presented in part at the 9th Annual Meeting of the Japanese Society of Dysphagia Rehabilitation.
References
Limitations of the study Several limitations of this study should be mentioned. First, due to the importance of keeping food and liquid in the mouth during the oral phase of swallowing, we selected a uniform experimental set-up in which the occlusal plane was parallel to the floor. While the 60 reclining posture is required in some dysphagia patients, the 60 chin-tuck position is not usually adopted in clinical practice. Moreover, several factors are important in selecting behavioural management besides keeping the occlusal plane parallel to the floor. It ª 2006 Blackwell Publishing Ltd, Journal of Oral Rehabilitation 33; 402–408
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