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The effect of a chin-down maneuver after esophagectomy on oropharyngeal swallowing pressure measured using high-resolution manometry
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The effect of a chin-down maneuver after esophagectomy on oropharyngeal swallowing pressure measured using high-resolution manometry$ Keigo Matsubara a, Yoshihiko Kumai b,*, Takumi Miyamoto b, Yasuhiro Samejima b, Naoya Yoshida c, Hideo Baba c, Yorihisa Orita b a
Department of Rehabilitations, Kumamoto Health Science University, Kumamoto, Japan Department of Otolaryngology Head and Neck Surgery, Kumamoto University Graduate School of Medicine, Kumamoto, Japan c Department of Gastroenterological Surgery, Kumamoto University Graduate School of Medicine, Japan b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 1 April 2019 Accepted 3 June 2019 Available online xxx
Objective: To elucidate the effects of a chin-down maneuver using high-resolution manometry (HRM) to measure pharyngeal swallowing pressure (SP) after esophagectomy. Methods: We evaluated 9 of 16 patients who underwent esophagectomy featuring gastric tube reconstruction and three-field lymph node dissection (3FL) in our Department of Gastroenterological Surgery from September 2015 to June 2016. We compared all parameters of the neutral and chindown positions using HRM to measure the maximum SP at the velopharynx, meso-hypopharynx, and upper esophageal sphincter (UES) and the duration of lowered SP at the UES, the distance from nostrils to the boundary between hypopharynx and UES and to derive SP and SP propagation curves at various distances from the nostrils. Results: Compared to that at the neutral position, the maximum SP at the velopharynx was significantly lower in the chin-down position (p < 0.05); however, SP at the meso-hypopharynx and UES did not differ significantly. The duration of lowered SP at the UES was significantly prolonged in the chin-down position and the distance from nostrils to the boundary between hypopharynx and UES was significantly shortened representing the elevation of the larynx, respectively (p < 0.05, p < 0.01). On the SP propagation curve for males, the times to SP peaks at 13, 16, 17, and 18 cm from the nostrils were significantly prolonged (all p < 0.05) in the chin-down position. Conclusion: Chin-down positioning after esophagectomy/3FL may improve bolus passage by prolonging the duration of lowered SP at the UES, possibly by enhancing laryngeal elevation. © 2019 Elsevier B.V. All rights reserved.
Keywords: High-resolution manometry Esophagectomy Three-field lymph node dissection Chin-down position Swallowing pressure Swallowing dysfunction Upper esophageal sphincter
1. Introduction Three-field lymphadenectomy (3FL) during esophagectomy to treat esophageal cancer, which is common in Japan, features $
JSPS KAKENHI Grant Number 15K10812. * Corresponding author at: Department of Otolaryngology Head and Neck Surgery, Kumamoto University School of Medicine, 860-8556 1-1-1 Honjo, Kumamoto, Japan. E-mail address: [email protected] (Y. Kumai).
complete dissection of the lymph nodes surrounding the recurrent laryngeal nerve (RLN) in the cervicothoracic region, an area associated with a high rate of metastasis [1]. This procedure may sometimes trigger pharyngeal swallowing dysfunctions and pulmonary complications, as scar tissue created in the cervicothoracic region impairs hyoid bone and laryngeal elevation, both of which are essential for normal swallowing [2,3]. Almost 40% of post-esophagectomy/3FL patients exhibited postoperative aspiration [4]. We previously performed a retrospective qualitative videofluoroscopic
https://doi.org/10.1016/j.anl.2019.06.001 0385-8146/© 2019 Elsevier B.V. All rights reserved.
Please cite this article in press as: Matsubara K, et al. The effect of a chin-down maneuver after esophagectomy on oropharyngeal swallowing pressure measured using high-resolution manometry. Auris Nasus Larynx (2019), https://doi.org/10.1016/j.anl.2019.06.001
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swallowing study (VFSS) and found that pharyngeal swallowing dysfunction in post-esophagectomy/3FL patients was significantly correlated with impaired laryngeal elevation [4]. In a second, prospective quantitative VFSS, we showed that the chin-down maneuver accelerated swallowing recovery by increasing pharyngeal constriction, reducing pharyngeal residue, opening the UES, and improving laryngeal closure [5]. In a third retrospective videoendoscopic swallowing study (VESS), we found that the chin-down maneuver usefully reduced the Penetration–Aspiration Scale (PAS) score and enhanced pharyngeal clearance in the pyriform sinus, especially in patients with vocal fold paralysis [6]. Based on these studies, we assumed that UES opening via cricopharyngeal muscle relaxation and/or an increase in pharyngeal swallowing pressure (SP) would be key in terms of the positive effects afforded by the chin-down maneuver in post-esophagectomy/ 3FL patients. Pharyngeal swallowing requires a complex series of coordinated muscle contractions, which generate SP gradients that move a food bolus from the pharynx to the esophagus. UES opening during normal swallowing is caused by (1) sphincter relaxation, (2) anterior laryngeal traction, and (3) Intra-bolus pressure produced by SP [7]. Therefore, to explore the specific cause of UES opening in the chin-down position observed in our earlier VFSS [5], the modulation of SP per se at both the pharynx and UES should be examined. However, it remains unclear how the maneuver might directly affect swallowing physiology, particularly pharyngeal SP, especially in dysphagic patients. High-resolution manometry (HRM) allows simultaneous pressure monitoring from the pharynx to the esophagus and plots the pressure topography using a 4.6-mm-diameter catheter featuring 36 circumferential sensors measuring pressures; the technique yields accurate pressure measurements in the asymmetrical pharynx during a single swallow. A few reports have explored the effects of compensatory maneuvers on SPs, especially in healthy subjects [8–10]; however, the detailed modulation of pharyngeal SP by such maneuvers in dysphagic patients remains unclear. Here, we used HRM to explore the effects of a chin-down maneuver on pharyngeal and UES SPs following esophagectomy/3FL. 2. Materials and methods Sixteen patients with thoracic esophageal cancer underwent esophagectomy/3FL and retrosternal esophageal reconstruction
using a gastric tube from September 2015 to June 2016 at the Department of Gastroenterological Surgery, Kumamoto University Hospital. Of these patients, only 10 (average age 68 years) agreed to undergo postoperative HRM. Written consent was obtained from all of these patients, who agreed that we could use their clinical data for diagnosis and pre-/ post-operative research evaluation. Ethical approval was granted by the Kumamoto University institutional review board (approval no. 2159). Esophagectomy featured lymphadenectomy accompanied by chest manipulation. If the tumor lay in the thoracic esophagus, 3FL was performed. The exclusion criterion was an upper thoracic esophageal tumor requiring UES resection (n = 1). We thus evaluated nine patients (6 male and 3 female) retrospectively. Table 1 shows the characteristics of all enrolled patients including sex, age, tumor location, tumor stage, recurrent laryngeal nerve paralysis status, and time to postoperative HRM. A solidstate device was used for all data collection. The Starlet HRM system (Star Medical, Inc., Tokyo, Japan) features a catheter with 36-channel solid-state sensors spaced at 1-cm intervals (Unisensor AG, Attikon, Switzerland). The sensors are unidirectional in nature and are covered with soft fluid-filled membranes. Luminal pressure depresses the membrane and is transferred to the fluid; the sensors thus perceive average luminal pressures in situ. The outer diameter of the thinnest part of the catheter is 4.0 mm, and that of each transducer site is 4.6 mm. Data were collected by a personal computer at a sampling frequency of 40 Hz which was initially set during manufacturing. The results are presented as pressure topographies (Fig. 1a,b) and waveforms (Fig. 2a). In addition, the software draws isobaric contours on the topographies (Fig. 1b) and measures the SP peaks and time to SP peaks in automated fashion. All subjects swallowed 2 mL of physiological saline in both the neutral and the chin-down positions (the latter with the neck flexed at the level of the lower cervical spine; the “neck flexion” position), as previously described [9,11]. Before commencing examinations, we asked all subjects to carefully assume the two positions following oral instructions (“please look straight ahead” for the neutral position and “please bend the neck forward as you do when you bow” for the chin-down position) and confirmed that they understood our requests. Swallowing was repeated three times at intervals of about 30 s. We administered topical anesthesia and a lubricant before inserting the catheter to reduce nasal and pharyngeal
Table 1 Characteristics of the enrolled patients. Patient no.
Sex
Age (y)
Tumor locarion
Tumor stage
RLN paralysis
Day of manometry (d)
1 2 3 4 5 6 7 8 9
M M M M M M F F F
71 71 65 68 59 75 77 59 65
L to Ae M L to Ae M to L M M M M M
III II II II I I IV II II
＋
15 15 17 17 18 18 18 17 17
Abbreviations:
＋ ＋ ＋ ＋
, negative; +, positve; L, lower; M, middle; Ae, abdominal; RLN, recurrent laryngeal nerve paralysis.
Please cite this article in press as: Matsubara K, et al. The effect of a chin-down maneuver after esophagectomy on oropharyngeal swallowing pressure measured using high-resolution manometry. Auris Nasus Larynx (2019), https://doi.org/10.1016/j.anl.2019.06.001
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Fig. 1. Representative data from an esophagectomized patient who underwent three-field (neck, mediastinal, and abdominal) lymphadenectomy (3FL); the patient swallowed 2 mL of physiological saline. Pressure topography: time on the x-axis (double-headed arrows: a = 5 s and b = 1 s); distance from the nostrils on the y-axis. Each pressure is assigned a color. The 20-mm Hg isobaric contours are shown (b). (A) Vocalization of “papapa.” (B) velopharynx, (C) meso-hypopharynx, and (D), the upper esophageal sphincter (UES). (E) The duration of lowered SP at the UES, i.e., the shortest time between the 20-mmHg isobaric contours associated with bolus passage. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fig. 2. (a) Pressure waveform: time on the x-axis (double-headed arrow: 1 s) and pressure on the y-axis. Black triangles: proportion of peak pressure at various distances from the nostrils. (b) Swallowing pressure (SP) curve obtained by plotting the maximum SPs at each point 9–18 cm distant from the nostrils. (c) SP propagation curve obtained by plotting the time to the SP peak by reference to the velopharyngeal peak.
discomfort. Before starting an examination, gauze impregnated with 4% (w/v) lidocaine hydrochloride was applied to the nasal passage for 5 min, followed by a cotton swab for 5 min. The catheter was lubricated with 2% (w/v) lidocaine jelly to ease passage through the nasal cavity. The catheter was inserted from the nostril to a point 41 cm into the esophagus and was taped to the nasal ala. The subjects then rested for about 5 min. A representative pressure topography is presented in Fig. 1. All subjects were asked to vocalize “papapa” prior to SP measurement to allow us to define the boundary between the velopharynx and the meso-hypopharynx (Fig.1a A). The topographic indicators showed that the pharyngeal pressure
was higher when swallowing than when vocalizing, as earlier indicated by Takasaki et al. [12]. The region of continuous high pressure in the center of the topographic map was the resting UES pressure; the boundary between the hypopharynx and UES was defined as the top edge of the high pressure region of the UES which always moves upward after elevation of the larynx during swallowing. We identified the upper UES region as the hypopharynx and the lower region as the cervical esophagus. The maximum SPs in the velopharynx (Fig. 1a B), mesohypopharynx (Fig. 1a C), and UES (Fig. 1a D), are shown. The duration of lowered SP at the UES was defined as the shortest elapsed time between the 20-mmHg isobaric contours for the bolus
Please cite this article in press as: Matsubara K, et al. The effect of a chin-down maneuver after esophagectomy on oropharyngeal swallowing pressure measured using high-resolution manometry. Auris Nasus Larynx (2019), https://doi.org/10.1016/j.anl.2019.06.001
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Fig. 3. Pressure topographies associated with the neutral and chin-down positions when two cases (Case a and b) swallowed 2 mL of physiological saline: neutral position (left): chin-down (right) position. The distance from nostrils to the boundary between hypopharynx and UES was significantly shortened due to the elevation of the larynx. The duration of lowered SP at the UES was obviously longer in the chin-down position. (For interpretation of the references to colour in the text, the reader is referred to the web version of this article.)
passage (Fig. 1b E). Fig. 3 shows that the pressure topographies differed significantly between the neutral and chin-down positions for two cases (Fig. 3a,b). The mean (averaged among three swallows) maximum SPs at the velopharynx, the mesohypopharynx, and the UES, as well as the durations of lowered SP at the UES and the distance from nostril to the boundary between hypopharynx and UES are measured in Table 2. SP curves were obtained by plotting the maximum SP from the nostrils to the cervical esophagus at 1 cm interval (Fig. 2a,b). The x-axis of an SP curve represents the maximum SP, and the y-axis is the distance from the nostril. SP propagation curves were created by plotting the duration to attainment of each SP peak by reference to the velopharyngeal peak (Fig. 2a,c). The x-axis on the SP propagation curve indicates the timing of the SP peak, and the y-axis is the distance from the nostrils. As the average pharyngeal length varies
by gender, separate SP and SP propagation curves were created for males and females (Figs. 4). The statistical differences between the neutral and chin-down positions (the p-values) at various distances from the nostrils in both the SP and SP propagation curves are listed separately for males and females (Tables 3 and 4) 3. Statistical analysis The Wilcoxon signed-rank test was used to compare the maximum SP values, duration of lowered SP at the UES, the distance from nostrils to the boundary between hypopharynx and UES the SP and SP propagation curves between the neutral and chin-down positions. A p-value <0.05 was deemed to reflect statistical significance. JMP ver. 14 software (SAS Institute, Inc., Cary, NC, USA) was used for all statistical analyses.
Table 2 Mean value of maximum swallowing pressure and the duration of lowered swallowing pressure at the UES. Parameters
Neutral position N = 9
Velopharynx (mmHg) Meso-hypopharynx (mmHg) UES (mmHg) The duration of lowered swallowing pressure at the UES (s) Boundary of meso-hypopharynx and UES (cm)
211.4 363.5 385.0 0.08 16.5
Chin-down position N = 9 33.9 111.0 104.8 0.09 1.9
201.9 367.6 387.9 0.16 15.9
34.2 118.8 125.1 0.09 1.9
p-Value 0.039 0.734 0.910 0.023 0.004
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Fig. 4. The average swallowing pressure (SP) and SP propagation curves for males (n = 6) and females (n = 3) who swallowed 2 mL of physiological saline. In males, the maximum SP at 20 cm distant from the nostrils was significantly lower in the chin-down compared to the neutral position. Compared to the neutral position, the times to the SP peaks at 13, 16, 17, and 18 cm from the nostrils were significantly prolonged in the chin-down position. In females, however, neither the SP nor SP propagation curve differed significantly between the two positions at any distance from the nostrils.
Table 3 Comparison of Swallowing pressure curve and propagation curve of 6 males.
Swallowing pressure curve (p value) Swallowing pressure propagation curve (p value)
10 cm
11 cm
12 cm
13 cm
14 cm
15 cm
16 cm
17 cm
18 cm
19 cm
20 cm
0.84 0.25
0.84 1.00
0.44 1.00
0.09 0.03
0.09 0.34
0.09 0.28
0.44 0.03
0.84 0.03
0.56 0.03
0.31 0.31
0.03 0.22
Table 4 Comparison of swallowing pressure curve and propagation curve of 3 females.
Swallowing pressure curve (p value) Swallowing pressure propagation curve (p value)
9 cm
10 cm
11 cm
12 cm
13 cm
14 cm
15 cm
16 cm
17 cm
1.00 0.50
1.00 0.25
0.25 1.00
0.50 1.00
0.25 1.00
0.50 1.00
0.75 0.75
0.25 1.00
0.25 1.00
4. Results Figs. 1 and 2 show typical pressure topographies and the SP and SP propagation curves, respectively. Fig. 3 reveals significant differences in the pressure topographies of the neutral and chin-down positions for two cases. Compared to the neutral position, the duration of lowered SP at the UES was prolonged in the chin-down position with partially lowered SP represented with diminished green zone at UES and the distance from nostrils to the boundary between hypopharynx and UES was shortened for both cases (Fig. 3). Compared to the neutral position, the maximum SP at the velopharynx was significantly lower (p < 0.05) in the chin-down position; however, the pressure at the meso-hypopharynx and UES did not differ between the two positions. The duration of lowered SP at the UES was significantly prolonged and the distance from nostrils to the boundary between hypopharynx and UES was significantly shortened due to the elevation of the larynx, respectively (p < 0.05, p < 0.01) (Table 2). On the males’ SP
curve of maximum chin-down SPs at 10–20 cm from the nostrils, the maximum SP at 20 cm was significantly lower (p < 0.05) in the chin-down position compared to the neutral position (Fig. 4 male, Table 3). On the males’ SP propagation curve, the time to the SP peaks at 13, 16, 17, and 18 cm from the nostrils were significantly longer (p < 0.05) in the chin-down position (Fig. 4 male, Table 3). However, for females, neither the SP nor SP propagation curve differed significantly at any distance from the nostrils in either position (Fig. 4 female, Table 4). 5. Discussion We earlier studied swallowing dysfunction and the positive effects of the chin-down maneuver in post-esophagectomy/3FL patients on both a VFSS and a VESS [4–6]. Based on these data, we hypothesized that UES opening via cricopharyngeal muscle relaxation and/or an increase in oropharyngeal SP triggered by laryngeal elevation would be key in terms of explaining the
Please cite this article in press as: Matsubara K, et al. The effect of a chin-down maneuver after esophagectomy on oropharyngeal swallowing pressure measured using high-resolution manometry. Auris Nasus Larynx (2019), https://doi.org/10.1016/j.anl.2019.06.001
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positive effects of the chin-down maneuver in postesophagectomy/3FL patients. To explore this hypothesis, we used HRM to measure pharyngeal and UES SPs during the chin-down maneuver in post-esophagectomy/3FL patients. Several studies have employed HRM to explore the effects of compensatory maneuvers on swallowing physiology in healthy volunteers but not in dysphagic patients [8–10]. We earlier showed that, in young healthy adults, a chin-down maneuver significantly lowered the maximum SP at the UES and increased the duration of lowered SP at the UES; this may assist in bolus passage [9]. However, any effect of this maneuver on the pharyngeal SP of dysphagic patients (such as post-esophagectomy/3FL patients) has not been well studied. Here, we explored the effects of the chin-down maneuver on the swallowing physiology of patients who had undergone esophagectomy/3FL, with a particular focus on modulation of the pharyngeal and UES SPs. UES opening during normal swallowing is caused by 1) sphincter relaxation, 2) anterior laryngeal traction, and 3) SP produced by intra-bolus passage [7]. The extended duration of UES opening in the chin-down position in post-esophagectomy/ 3FL patients evaluated in our earlier VFSS might be attributable to improvement in one of the above three factors. In the present study we found that, compared to the neutral position, the maximum SP at the velopharynx was significantly lower (p < 0.05) in the chin-down position, but this was not the case at the meso-hypopharynx or UES (Table 2). We thus assume that an increased intra-bolus pressure produced by SP might not be the principal cause of UES opening time extension. Interestingly, the duration of lowered SP at the UES was significantly prolonged (p < 0.05) in the chin-down position compared to the neutral position (Table 2), supporting our earlier manometric findings in healthy young adults [9]. This earlier work also showed that, in young healthy adults, a chin-down maneuver significantly increased the duration of lowered SP at the UES, which may assist in bolus passage [9]. Based on these data, a significantly prolonged duration of lowered SP during UES relaxation might be the principal reason that UES opening time was extended in our earlier VFSS study. We also found that, on the curve of maximum SPs 10–20 cm from the nostrils in males, the maximum SP at 20 cm was significantly lower (p < 0.05) in the chin-down compared to the neutral position (Fig. 4 male, Table 3). Coordinated, continuous swallowing-associated muscular contractions associated with bolus passage from the pharynx to the esophagus are controlled by the central pattern generator of the medulla oblongata. Thus, the SP propagation curve is usually very reproducible regardless of the bolus amount [13]. An abnormal SP propagation curve reflects a disorder of preprogrammed swallowing, such as brainstem damage caused by cerebrovascular disease [14,15]. Esophagectomized patients obviously lack such damage; their patterns were basically identical to those of healthy young adults [16]. However, in the present study, on the SP propagation curve for males (n = 6), the time to peak SP at 16, 17, and 18 cm from the nostrils were significantly prolonged (p < 0.05) in the chin-down compared to the neutral position (Fig. 4 male, Table 3) Since the length of the pharynx differs individually, the distance from the nostrils
cannot specify the exact anatomical location. Among the six male patients in the present study, boundary between hypopharynx and UES was located between 16 and 17 cm from the nostrils for two patients, between 17 and 18 cm for two patients and between 18 and 19 cm for one patient, suggesting that among all six patients, UES or boundary between hypopharynx and UES were located at 16, 17 and 18 cm from the nostrils at which the time to the SP peaks were significantly longer (p < 0.05) in the chin-down maneuver. Additionally, the distance from nostrils to the boundary between hypopharynx and UES was significantly shortened (p < 0.01) representing the elevation of the larynx. Karaho [17] previously demonstrated that chin-down maneuver shifted the pressure sensor of the manometry upward and consequently the pressure at UES was measured by the caudal sensor than that during neutral position. Based on the present data and the previous perspective, we assume that HRM detected an SP at a UES that had been elevated (together with the larynx) during chin-down swallowing. As our earlier VFSS showed that the chin-down position is assumed to improve laryngeal elevation in esophagectomized patients [5] and McConnel FM demonstrated that the bolus transit is dependent upon tongue driving pressure and the negative pressure developed in the pharyngeal esophageal segment as a hypopharyngeal suction pump [18]. The data of the present study and the previous perspective support the notion that the maneuver likely increases the extent of UES opening with accelerated hypopharyngeal suction pump and smooths bolus passage via laryngeal elevation. In esophagectomy/3FL patients, scar tissue in the cervicothoracic region impairs hyoid bone and/or laryngeal elevation, which are key in terms of normal swallowing [2,3]. The chin-down maneuver would induce strap muscle relaxation [19] and promotes laryngeal elevation, in turn prolonging the duration of UES opening. Thus, the maneuver extends the duration of UES opening with smooths bolus passage not by intra-bolus pressure produced by SP at mesohypopharynx but by a combination of laryngeal elevation and a significant prolongation of UES relaxation with accelerated hypopharyngeal suction pump. 6. Limitations There are several limitations in the present study. First is that only a few patients agreed to undergo postoperative HRM in the present study; more patient number is required for the statistically precise analysis. Then, enhancement of factors related to the patient characterization such as sex, age, tumor location, tumor size, type of reconstruction procedure for gastric tube and the presence or absence of recurrent laryngeal nerve paralysis on the effect of chin-down maneuver needs to be further speculated in the future with statistically sufficient number of patients. Secondly, we did not combine HRM with a VFSS; this limitation will be addressed in the future. Third, sampling frequency of 40 Hz is insufficient for precisely capturing steep pressure changes in the hypopharynx, therefore, setting the high sampling frequency (e.g.100 Hz) would be necessary in the future.
Please cite this article in press as: Matsubara K, et al. The effect of a chin-down maneuver after esophagectomy on oropharyngeal swallowing pressure measured using high-resolution manometry. Auris Nasus Larynx (2019), https://doi.org/10.1016/j.anl.2019.06.001
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7. Conclusion Assumption of a chin-down position after esophagectomy/ 3FL may improve bolus passage by prolonging the duration of reduced SP at the UES, mediated by enhanced laryngeal elevation. Financial disclosure None. Conflict of interest None. Level of evidence: IV. References [1] Altorki N, Kent M, Ferrara C, Port J. Three-field lymph node dissection for squamous cell and adenocarcinoma of the esophagus. Ann Surg 2002;236(2):177–83. [2] Yasuda T, Yano M, Miyata H, Yamasaki M, Takiguchi S, Fujiwara Y, et al. Evaluation of dysphagia and diminished airway protection after three-field esophagectomy and a remedy. World J Surg 2013;37 (2):416–23. [3] Kato H, Miyazaki T, Sakai M, Sano A, Tanaka N, Kimura H, et al. Videofluoroscopic evaluation in oropharyngeal swallowing after radical esophagectomy with lymphadenectomy for esophageal cancer. Anticancer Res 2007;27(6C):4249–54. [4] Kumai Y, Samejima Y, Watanabe M, Yumoto E. Videofluoroscopic evaluation of pharyngeal swallowing dysfunction after esophagectomy with three-field lymph node dissection. Eur Arch Otorhinolaryngol 2017;274(1):321–6. [5] Kumai Y, Yoshida N, Kamenosono Y, Matsubara K, Samejima Y, Baba H, et al. effects of chin-down maneuver on the parameters of swallowing function after esophagectomy with 3-field lymphadenectomy examined by videofluoroscopy. Arch Phys Med Rehabil 2017;98 (6):1174–9.
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The effect of a chin-down maneuver after esophagectomy on oropharyngeal swallowing pressure measured using high-resolution manometry$ Keigo Matsubara a, Yoshihiko Kumai b,*, Takumi Miyamoto b, Yasuhiro Samejima b, Naoya Yoshida c, Hideo Baba c, Yorihisa Orita b a
Department of Rehabilitations, Kumamoto Health Science University, Kumamoto, Japan Department of Otolaryngology Head and Neck Surgery, Kumamoto University Graduate School of Medicine, Kumamoto, Japan c Department of Gastroenterological Surgery, Kumamoto University Graduate School of Medicine, Japan b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 1 April 2019 Accepted 3 June 2019 Available online xxx
Objective: To elucidate the effects of a chin-down maneuver using high-resolution manometry (HRM) to measure pharyngeal swallowing pressure (SP) after esophagectomy. Methods: We evaluated 9 of 16 patients who underwent esophagectomy featuring gastric tube reconstruction and three-field lymph node dissection (3FL) in our Department of Gastroenterological Surgery from September 2015 to June 2016. We compared all parameters of the neutral and chindown positions using HRM to measure the maximum SP at the velopharynx, meso-hypopharynx, and upper esophageal sphincter (UES) and the duration of lowered SP at the UES, the distance from nostrils to the boundary between hypopharynx and UES and to derive SP and SP propagation curves at various distances from the nostrils. Results: Compared to that at the neutral position, the maximum SP at the velopharynx was significantly lower in the chin-down position (p < 0.05); however, SP at the meso-hypopharynx and UES did not differ significantly. The duration of lowered SP at the UES was significantly prolonged in the chin-down position and the distance from nostrils to the boundary between hypopharynx and UES was significantly shortened representing the elevation of the larynx, respectively (p < 0.05, p < 0.01). On the SP propagation curve for males, the times to SP peaks at 13, 16, 17, and 18 cm from the nostrils were significantly prolonged (all p < 0.05) in the chin-down position. Conclusion: Chin-down positioning after esophagectomy/3FL may improve bolus passage by prolonging the duration of lowered SP at the UES, possibly by enhancing laryngeal elevation. © 2019 Elsevier B.V. All rights reserved.
Keywords: High-resolution manometry Esophagectomy Three-field lymph node dissection Chin-down position Swallowing pressure Swallowing dysfunction Upper esophageal sphincter
1. Introduction Three-field lymphadenectomy (3FL) during esophagectomy to treat esophageal cancer, which is common in Japan, features $
JSPS KAKENHI Grant Number 15K10812. * Corresponding author at: Department of Otolaryngology Head and Neck Surgery, Kumamoto University School of Medicine, 860-8556 1-1-1 Honjo, Kumamoto, Japan. E-mail address: [email protected] (Y. Kumai).
complete dissection of the lymph nodes surrounding the recurrent laryngeal nerve (RLN) in the cervicothoracic region, an area associated with a high rate of metastasis [1]. This procedure may sometimes trigger pharyngeal swallowing dysfunctions and pulmonary complications, as scar tissue created in the cervicothoracic region impairs hyoid bone and laryngeal elevation, both of which are essential for normal swallowing [2,3]. Almost 40% of post-esophagectomy/3FL patients exhibited postoperative aspiration [4]. We previously performed a retrospective qualitative videofluoroscopic
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Please cite this article in press as: Matsubara K, et al. The effect of a chin-down maneuver after esophagectomy on oropharyngeal swallowing pressure measured using high-resolution manometry. Auris Nasus Larynx (2019), https://doi.org/10.1016/j.anl.2019.06.001
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swallowing study (VFSS) and found that pharyngeal swallowing dysfunction in post-esophagectomy/3FL patients was significantly correlated with impaired laryngeal elevation [4]. In a second, prospective quantitative VFSS, we showed that the chin-down maneuver accelerated swallowing recovery by increasing pharyngeal constriction, reducing pharyngeal residue, opening the UES, and improving laryngeal closure [5]. In a third retrospective videoendoscopic swallowing study (VESS), we found that the chin-down maneuver usefully reduced the Penetration–Aspiration Scale (PAS) score and enhanced pharyngeal clearance in the pyriform sinus, especially in patients with vocal fold paralysis [6]. Based on these studies, we assumed that UES opening via cricopharyngeal muscle relaxation and/or an increase in pharyngeal swallowing pressure (SP) would be key in terms of the positive effects afforded by the chin-down maneuver in post-esophagectomy/ 3FL patients. Pharyngeal swallowing requires a complex series of coordinated muscle contractions, which generate SP gradients that move a food bolus from the pharynx to the esophagus. UES opening during normal swallowing is caused by (1) sphincter relaxation, (2) anterior laryngeal traction, and (3) Intra-bolus pressure produced by SP [7]. Therefore, to explore the specific cause of UES opening in the chin-down position observed in our earlier VFSS [5], the modulation of SP per se at both the pharynx and UES should be examined. However, it remains unclear how the maneuver might directly affect swallowing physiology, particularly pharyngeal SP, especially in dysphagic patients. High-resolution manometry (HRM) allows simultaneous pressure monitoring from the pharynx to the esophagus and plots the pressure topography using a 4.6-mm-diameter catheter featuring 36 circumferential sensors measuring pressures; the technique yields accurate pressure measurements in the asymmetrical pharynx during a single swallow. A few reports have explored the effects of compensatory maneuvers on SPs, especially in healthy subjects [8–10]; however, the detailed modulation of pharyngeal SP by such maneuvers in dysphagic patients remains unclear. Here, we used HRM to explore the effects of a chin-down maneuver on pharyngeal and UES SPs following esophagectomy/3FL. 2. Materials and methods Sixteen patients with thoracic esophageal cancer underwent esophagectomy/3FL and retrosternal esophageal reconstruction
using a gastric tube from September 2015 to June 2016 at the Department of Gastroenterological Surgery, Kumamoto University Hospital. Of these patients, only 10 (average age 68 years) agreed to undergo postoperative HRM. Written consent was obtained from all of these patients, who agreed that we could use their clinical data for diagnosis and pre-/ post-operative research evaluation. Ethical approval was granted by the Kumamoto University institutional review board (approval no. 2159). Esophagectomy featured lymphadenectomy accompanied by chest manipulation. If the tumor lay in the thoracic esophagus, 3FL was performed. The exclusion criterion was an upper thoracic esophageal tumor requiring UES resection (n = 1). We thus evaluated nine patients (6 male and 3 female) retrospectively. Table 1 shows the characteristics of all enrolled patients including sex, age, tumor location, tumor stage, recurrent laryngeal nerve paralysis status, and time to postoperative HRM. A solidstate device was used for all data collection. The Starlet HRM system (Star Medical, Inc., Tokyo, Japan) features a catheter with 36-channel solid-state sensors spaced at 1-cm intervals (Unisensor AG, Attikon, Switzerland). The sensors are unidirectional in nature and are covered with soft fluid-filled membranes. Luminal pressure depresses the membrane and is transferred to the fluid; the sensors thus perceive average luminal pressures in situ. The outer diameter of the thinnest part of the catheter is 4.0 mm, and that of each transducer site is 4.6 mm. Data were collected by a personal computer at a sampling frequency of 40 Hz which was initially set during manufacturing. The results are presented as pressure topographies (Fig. 1a,b) and waveforms (Fig. 2a). In addition, the software draws isobaric contours on the topographies (Fig. 1b) and measures the SP peaks and time to SP peaks in automated fashion. All subjects swallowed 2 mL of physiological saline in both the neutral and the chin-down positions (the latter with the neck flexed at the level of the lower cervical spine; the “neck flexion” position), as previously described [9,11]. Before commencing examinations, we asked all subjects to carefully assume the two positions following oral instructions (“please look straight ahead” for the neutral position and “please bend the neck forward as you do when you bow” for the chin-down position) and confirmed that they understood our requests. Swallowing was repeated three times at intervals of about 30 s. We administered topical anesthesia and a lubricant before inserting the catheter to reduce nasal and pharyngeal
Table 1 Characteristics of the enrolled patients. Patient no.
Sex
Age (y)
Tumor locarion
Tumor stage
RLN paralysis
Day of manometry (d)
1 2 3 4 5 6 7 8 9
M M M M M M F F F
71 71 65 68 59 75 77 59 65
L to Ae M L to Ae M to L M M M M M
III II II II I I IV II II
＋
15 15 17 17 18 18 18 17 17
Abbreviations:
＋ ＋ ＋ ＋
, negative; +, positve; L, lower; M, middle; Ae, abdominal; RLN, recurrent laryngeal nerve paralysis.
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Fig. 1. Representative data from an esophagectomized patient who underwent three-field (neck, mediastinal, and abdominal) lymphadenectomy (3FL); the patient swallowed 2 mL of physiological saline. Pressure topography: time on the x-axis (double-headed arrows: a = 5 s and b = 1 s); distance from the nostrils on the y-axis. Each pressure is assigned a color. The 20-mm Hg isobaric contours are shown (b). (A) Vocalization of “papapa.” (B) velopharynx, (C) meso-hypopharynx, and (D), the upper esophageal sphincter (UES). (E) The duration of lowered SP at the UES, i.e., the shortest time between the 20-mmHg isobaric contours associated with bolus passage. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fig. 2. (a) Pressure waveform: time on the x-axis (double-headed arrow: 1 s) and pressure on the y-axis. Black triangles: proportion of peak pressure at various distances from the nostrils. (b) Swallowing pressure (SP) curve obtained by plotting the maximum SPs at each point 9–18 cm distant from the nostrils. (c) SP propagation curve obtained by plotting the time to the SP peak by reference to the velopharyngeal peak.
discomfort. Before starting an examination, gauze impregnated with 4% (w/v) lidocaine hydrochloride was applied to the nasal passage for 5 min, followed by a cotton swab for 5 min. The catheter was lubricated with 2% (w/v) lidocaine jelly to ease passage through the nasal cavity. The catheter was inserted from the nostril to a point 41 cm into the esophagus and was taped to the nasal ala. The subjects then rested for about 5 min. A representative pressure topography is presented in Fig. 1. All subjects were asked to vocalize “papapa” prior to SP measurement to allow us to define the boundary between the velopharynx and the meso-hypopharynx (Fig.1a A). The topographic indicators showed that the pharyngeal pressure
was higher when swallowing than when vocalizing, as earlier indicated by Takasaki et al. [12]. The region of continuous high pressure in the center of the topographic map was the resting UES pressure; the boundary between the hypopharynx and UES was defined as the top edge of the high pressure region of the UES which always moves upward after elevation of the larynx during swallowing. We identified the upper UES region as the hypopharynx and the lower region as the cervical esophagus. The maximum SPs in the velopharynx (Fig. 1a B), mesohypopharynx (Fig. 1a C), and UES (Fig. 1a D), are shown. The duration of lowered SP at the UES was defined as the shortest elapsed time between the 20-mmHg isobaric contours for the bolus
Please cite this article in press as: Matsubara K, et al. The effect of a chin-down maneuver after esophagectomy on oropharyngeal swallowing pressure measured using high-resolution manometry. Auris Nasus Larynx (2019), https://doi.org/10.1016/j.anl.2019.06.001
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Fig. 3. Pressure topographies associated with the neutral and chin-down positions when two cases (Case a and b) swallowed 2 mL of physiological saline: neutral position (left): chin-down (right) position. The distance from nostrils to the boundary between hypopharynx and UES was significantly shortened due to the elevation of the larynx. The duration of lowered SP at the UES was obviously longer in the chin-down position. (For interpretation of the references to colour in the text, the reader is referred to the web version of this article.)
passage (Fig. 1b E). Fig. 3 shows that the pressure topographies differed significantly between the neutral and chin-down positions for two cases (Fig. 3a,b). The mean (averaged among three swallows) maximum SPs at the velopharynx, the mesohypopharynx, and the UES, as well as the durations of lowered SP at the UES and the distance from nostril to the boundary between hypopharynx and UES are measured in Table 2. SP curves were obtained by plotting the maximum SP from the nostrils to the cervical esophagus at 1 cm interval (Fig. 2a,b). The x-axis of an SP curve represents the maximum SP, and the y-axis is the distance from the nostril. SP propagation curves were created by plotting the duration to attainment of each SP peak by reference to the velopharyngeal peak (Fig. 2a,c). The x-axis on the SP propagation curve indicates the timing of the SP peak, and the y-axis is the distance from the nostrils. As the average pharyngeal length varies
by gender, separate SP and SP propagation curves were created for males and females (Figs. 4). The statistical differences between the neutral and chin-down positions (the p-values) at various distances from the nostrils in both the SP and SP propagation curves are listed separately for males and females (Tables 3 and 4) 3. Statistical analysis The Wilcoxon signed-rank test was used to compare the maximum SP values, duration of lowered SP at the UES, the distance from nostrils to the boundary between hypopharynx and UES the SP and SP propagation curves between the neutral and chin-down positions. A p-value <0.05 was deemed to reflect statistical significance. JMP ver. 14 software (SAS Institute, Inc., Cary, NC, USA) was used for all statistical analyses.
Table 2 Mean value of maximum swallowing pressure and the duration of lowered swallowing pressure at the UES. Parameters
Neutral position N = 9
Velopharynx (mmHg) Meso-hypopharynx (mmHg) UES (mmHg) The duration of lowered swallowing pressure at the UES (s) Boundary of meso-hypopharynx and UES (cm)
211.4 363.5 385.0 0.08 16.5
Chin-down position N = 9 33.9 111.0 104.8 0.09 1.9
201.9 367.6 387.9 0.16 15.9
34.2 118.8 125.1 0.09 1.9
p-Value 0.039 0.734 0.910 0.023 0.004
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Fig. 4. The average swallowing pressure (SP) and SP propagation curves for males (n = 6) and females (n = 3) who swallowed 2 mL of physiological saline. In males, the maximum SP at 20 cm distant from the nostrils was significantly lower in the chin-down compared to the neutral position. Compared to the neutral position, the times to the SP peaks at 13, 16, 17, and 18 cm from the nostrils were significantly prolonged in the chin-down position. In females, however, neither the SP nor SP propagation curve differed significantly between the two positions at any distance from the nostrils.
Table 3 Comparison of Swallowing pressure curve and propagation curve of 6 males.
Swallowing pressure curve (p value) Swallowing pressure propagation curve (p value)
10 cm
11 cm
12 cm
13 cm
14 cm
15 cm
16 cm
17 cm
18 cm
19 cm
20 cm
0.84 0.25
0.84 1.00
0.44 1.00
0.09 0.03
0.09 0.34
0.09 0.28
0.44 0.03
0.84 0.03
0.56 0.03
0.31 0.31
0.03 0.22
Table 4 Comparison of swallowing pressure curve and propagation curve of 3 females.
Swallowing pressure curve (p value) Swallowing pressure propagation curve (p value)
9 cm
10 cm
11 cm
12 cm
13 cm
14 cm
15 cm
16 cm
17 cm
1.00 0.50
1.00 0.25
0.25 1.00
0.50 1.00
0.25 1.00
0.50 1.00
0.75 0.75
0.25 1.00
0.25 1.00
4. Results Figs. 1 and 2 show typical pressure topographies and the SP and SP propagation curves, respectively. Fig. 3 reveals significant differences in the pressure topographies of the neutral and chin-down positions for two cases. Compared to the neutral position, the duration of lowered SP at the UES was prolonged in the chin-down position with partially lowered SP represented with diminished green zone at UES and the distance from nostrils to the boundary between hypopharynx and UES was shortened for both cases (Fig. 3). Compared to the neutral position, the maximum SP at the velopharynx was significantly lower (p < 0.05) in the chin-down position; however, the pressure at the meso-hypopharynx and UES did not differ between the two positions. The duration of lowered SP at the UES was significantly prolonged and the distance from nostrils to the boundary between hypopharynx and UES was significantly shortened due to the elevation of the larynx, respectively (p < 0.05, p < 0.01) (Table 2). On the males’ SP
curve of maximum chin-down SPs at 10–20 cm from the nostrils, the maximum SP at 20 cm was significantly lower (p < 0.05) in the chin-down position compared to the neutral position (Fig. 4 male, Table 3). On the males’ SP propagation curve, the time to the SP peaks at 13, 16, 17, and 18 cm from the nostrils were significantly longer (p < 0.05) in the chin-down position (Fig. 4 male, Table 3). However, for females, neither the SP nor SP propagation curve differed significantly at any distance from the nostrils in either position (Fig. 4 female, Table 4). 5. Discussion We earlier studied swallowing dysfunction and the positive effects of the chin-down maneuver in post-esophagectomy/3FL patients on both a VFSS and a VESS [4–6]. Based on these data, we hypothesized that UES opening via cricopharyngeal muscle relaxation and/or an increase in oropharyngeal SP triggered by laryngeal elevation would be key in terms of explaining the
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positive effects of the chin-down maneuver in postesophagectomy/3FL patients. To explore this hypothesis, we used HRM to measure pharyngeal and UES SPs during the chin-down maneuver in post-esophagectomy/3FL patients. Several studies have employed HRM to explore the effects of compensatory maneuvers on swallowing physiology in healthy volunteers but not in dysphagic patients [8–10]. We earlier showed that, in young healthy adults, a chin-down maneuver significantly lowered the maximum SP at the UES and increased the duration of lowered SP at the UES; this may assist in bolus passage [9]. However, any effect of this maneuver on the pharyngeal SP of dysphagic patients (such as post-esophagectomy/3FL patients) has not been well studied. Here, we explored the effects of the chin-down maneuver on the swallowing physiology of patients who had undergone esophagectomy/3FL, with a particular focus on modulation of the pharyngeal and UES SPs. UES opening during normal swallowing is caused by 1) sphincter relaxation, 2) anterior laryngeal traction, and 3) SP produced by intra-bolus passage [7]. The extended duration of UES opening in the chin-down position in post-esophagectomy/ 3FL patients evaluated in our earlier VFSS might be attributable to improvement in one of the above three factors. In the present study we found that, compared to the neutral position, the maximum SP at the velopharynx was significantly lower (p < 0.05) in the chin-down position, but this was not the case at the meso-hypopharynx or UES (Table 2). We thus assume that an increased intra-bolus pressure produced by SP might not be the principal cause of UES opening time extension. Interestingly, the duration of lowered SP at the UES was significantly prolonged (p < 0.05) in the chin-down position compared to the neutral position (Table 2), supporting our earlier manometric findings in healthy young adults [9]. This earlier work also showed that, in young healthy adults, a chin-down maneuver significantly increased the duration of lowered SP at the UES, which may assist in bolus passage [9]. Based on these data, a significantly prolonged duration of lowered SP during UES relaxation might be the principal reason that UES opening time was extended in our earlier VFSS study. We also found that, on the curve of maximum SPs 10–20 cm from the nostrils in males, the maximum SP at 20 cm was significantly lower (p < 0.05) in the chin-down compared to the neutral position (Fig. 4 male, Table 3). Coordinated, continuous swallowing-associated muscular contractions associated with bolus passage from the pharynx to the esophagus are controlled by the central pattern generator of the medulla oblongata. Thus, the SP propagation curve is usually very reproducible regardless of the bolus amount [13]. An abnormal SP propagation curve reflects a disorder of preprogrammed swallowing, such as brainstem damage caused by cerebrovascular disease [14,15]. Esophagectomized patients obviously lack such damage; their patterns were basically identical to those of healthy young adults [16]. However, in the present study, on the SP propagation curve for males (n = 6), the time to peak SP at 16, 17, and 18 cm from the nostrils were significantly prolonged (p < 0.05) in the chin-down compared to the neutral position (Fig. 4 male, Table 3) Since the length of the pharynx differs individually, the distance from the nostrils
cannot specify the exact anatomical location. Among the six male patients in the present study, boundary between hypopharynx and UES was located between 16 and 17 cm from the nostrils for two patients, between 17 and 18 cm for two patients and between 18 and 19 cm for one patient, suggesting that among all six patients, UES or boundary between hypopharynx and UES were located at 16, 17 and 18 cm from the nostrils at which the time to the SP peaks were significantly longer (p < 0.05) in the chin-down maneuver. Additionally, the distance from nostrils to the boundary between hypopharynx and UES was significantly shortened (p < 0.01) representing the elevation of the larynx. Karaho [17] previously demonstrated that chin-down maneuver shifted the pressure sensor of the manometry upward and consequently the pressure at UES was measured by the caudal sensor than that during neutral position. Based on the present data and the previous perspective, we assume that HRM detected an SP at a UES that had been elevated (together with the larynx) during chin-down swallowing. As our earlier VFSS showed that the chin-down position is assumed to improve laryngeal elevation in esophagectomized patients [5] and McConnel FM demonstrated that the bolus transit is dependent upon tongue driving pressure and the negative pressure developed in the pharyngeal esophageal segment as a hypopharyngeal suction pump [18]. The data of the present study and the previous perspective support the notion that the maneuver likely increases the extent of UES opening with accelerated hypopharyngeal suction pump and smooths bolus passage via laryngeal elevation. In esophagectomy/3FL patients, scar tissue in the cervicothoracic region impairs hyoid bone and/or laryngeal elevation, which are key in terms of normal swallowing [2,3]. The chin-down maneuver would induce strap muscle relaxation [19] and promotes laryngeal elevation, in turn prolonging the duration of UES opening. Thus, the maneuver extends the duration of UES opening with smooths bolus passage not by intra-bolus pressure produced by SP at mesohypopharynx but by a combination of laryngeal elevation and a significant prolongation of UES relaxation with accelerated hypopharyngeal suction pump. 6. Limitations There are several limitations in the present study. First is that only a few patients agreed to undergo postoperative HRM in the present study; more patient number is required for the statistically precise analysis. Then, enhancement of factors related to the patient characterization such as sex, age, tumor location, tumor size, type of reconstruction procedure for gastric tube and the presence or absence of recurrent laryngeal nerve paralysis on the effect of chin-down maneuver needs to be further speculated in the future with statistically sufficient number of patients. Secondly, we did not combine HRM with a VFSS; this limitation will be addressed in the future. Third, sampling frequency of 40 Hz is insufficient for precisely capturing steep pressure changes in the hypopharynx, therefore, setting the high sampling frequency (e.g.100 Hz) would be necessary in the future.
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7. Conclusion Assumption of a chin-down position after esophagectomy/ 3FL may improve bolus passage by prolonging the duration of reduced SP at the UES, mediated by enhanced laryngeal elevation. Financial disclosure None. Conflict of interest None. Level of evidence: IV. References [1] Altorki N, Kent M, Ferrara C, Port J. Three-field lymph node dissection for squamous cell and adenocarcinoma of the esophagus. Ann Surg 2002;236(2):177–83. [2] Yasuda T, Yano M, Miyata H, Yamasaki M, Takiguchi S, Fujiwara Y, et al. Evaluation of dysphagia and diminished airway protection after three-field esophagectomy and a remedy. World J Surg 2013;37 (2):416–23. [3] Kato H, Miyazaki T, Sakai M, Sano A, Tanaka N, Kimura H, et al. Videofluoroscopic evaluation in oropharyngeal swallowing after radical esophagectomy with lymphadenectomy for esophageal cancer. Anticancer Res 2007;27(6C):4249–54. [4] Kumai Y, Samejima Y, Watanabe M, Yumoto E. Videofluoroscopic evaluation of pharyngeal swallowing dysfunction after esophagectomy with three-field lymph node dissection. Eur Arch Otorhinolaryngol 2017;274(1):321–6. [5] Kumai Y, Yoshida N, Kamenosono Y, Matsubara K, Samejima Y, Baba H, et al. effects of chin-down maneuver on the parameters of swallowing function after esophagectomy with 3-field lymphadenectomy examined by videofluoroscopy. Arch Phys Med Rehabil 2017;98 (6):1174–9.
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Please cite this article in press as: Matsubara K, et al. The effect of a chin-down maneuver after esophagectomy on oropharyngeal swallowing pressure measured using high-resolution manometry. Auris Nasus Larynx (2019), https://doi.org/10.1016/j.anl.2019.06.001