Acta Oto-Laryngologica. 2015; 135: 187–192
ORIGINAL ARTICLE
Can mano-videoendoscopy substitute for videofluorography in evaluation of upper esophageal sphincter function?
TAKEHIRO KARAHO1,2, TETSUYA SATOH1,2, JUNKO NAKAJIMA2,3, TAKESHI NAKAYAMA2,4 & NAOYUKI KOHNO1 PRESENTED AT THE 36TH ANNUAL CONFERENCE OF THE SOCIETY OF SWALLOWING AND DYSPHAGIA OF JAPAN, KYOTO, MARCH 1–2, 2013. 1
Department of Otolaryngology Head and Neck Surgery, Kyorin University, School of Medicine, Mitaka, Tokyo, 2Kyorin University Hospital Swallowing Center, Mitaka, Tokyo, 3Department of Oral and Maxillofacial Surgery, National Defense Medical College, Tokorozawa, Saitama and 4Japan Welfare Education College, Shinjuku, Tokyo, Japan
Abstract Conclusions: Mano-videoendoscopy (MVE), a manometry technique with endoscopic confirmation of the pressure catheter, can supplement the information on upper esophageal sphincter (UES) function, and overcomes the drawbacks of videoendoscopic swallowing study (VESS). Objectives: This study aimed to investigate the possibility of replacing videofluorographic swallowing study (VFSS) with MVE, as a test to precisely evaluate UES function. Methods: Data from 52 patients with dysphagia were retrospectively reviewed. All patients underwent both MVE and VFSS for evaluation of dysphagia. The manometry was performed with a transnasally inserted catheter (2.6 mm outer diameter and four pressure sensors) under endoscopic observation. The sensors were kept at the tongue base, upper pyriform sinus, apex of pyriform sinus, and UES. We statistically compared the manometric parameters of UES relaxation with fluorographic UES opening. Results: Fluorographic UES opening was diagnosed as good in 34 patients and poor in 18 patients. The nadir pressure, pressure drop, and pressure rise in the UES had significant correlation on the fluorographic UES opening. Stepwise logistic regression test revealed that pressure drop, the gap between the resting pressure and the nadir of UES pressure, was a robust parameter for predicting fluorographic UES opening, and the cut-off level to anticipate good fluorographic opening was ‡ 33.5 mmHg (specificity, 0.853; sensitivity, 0.759)
Keywords: swallowing study, fluorography, dysphagia
Introduction Videoendoscopic swallowing studies (VESS) have become the standard method for examining the swallowing function in patients with dysphagia, because the procedure is relatively non-invasive and can even be performed at the patient’s bedside. Initially, it was performed mostly in patients who could not be adequately examined with videofluorographic swallowing studies (VFSS), which is viewed as the gold standard of swallowing function tests [1]. However, due to their portability and convenient use,
endoscopic examinations are now performed at some institutions as a test of swallowing function in place of videofluorography [2,3]. In institutions where both examinations can be performed, VESS and VFSS are generally used complementarily [3]. Compared with videofluorography, endoscopic examination has the disadvantages of not allowing visualization of the oral and esophageal stages of swallowing, the pharyngeal contraction cannot be objectively evaluated, and the opening (relaxation) of the upper esophageal sphincter (UES) cannot be observed [3]. The opening of the UES is a
Correspondence: Takehiro Karaho, Department of Otolaryngology Head and Neck Surgery, Kyorin University, School of Medicine, 6-20-2, Shinkawa, Mitaka, Tokyo, 181-8611, Japan. Tel: +81 422 47 5511. E-mail: [email protected]
(Received 19 July 2014; accepted 4 September 2014) ISSN 0001-6489 print/ISSN 1651-2251 online 2015 Informa Healthcare DOI: 10.3109/00016489.2014.969384
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phenomenon that occurs as a result of the relaxation of the cricopharyngeal muscle and laryngeal elevation, although the opening and relaxation of the sphincter do not occur at exactly the same time [4,5]. Information about the presence or absence of UES opening (relaxation) is especially important, as it affects the subsequent treatment strategy, and examinations that cannot evaluate this are inadequate as examinations of the swallowing function. Manometry, which is used to measure the pressure in the pharynx and esophagus during swallowing, enables the observation of the swallowing pressure, which indicates the force of the propulsion of a bolus of food at the level of the base of the tongue, and the relaxation status of the UES [4–6]. However, pressure waveforms differ depending on the positions in which the solid-state sensors are placed. In patients with pharyngeal dysphagia, the pressure catheter is sometimes accidentally inserted into the larynx rather than the esophagus. Since it is therefore advisable to confirm the position of the solid-state sensors during examination, videofluorography is usually performed simultaneously with manometry [4,5]. In such cases, however, the radiation exposure is a problem. Mano-videoendoscopy (MVE) is a technique used to obtain additional manometric information, for example, information about pharyngeal contraction and UES relaxation, after a routine VESS examination [7]. This procedure may reduce the VFSS for the purpose of analyzing the UES function. The aim of the present study was to investigate the possibility of replacing VFSS with MVE, which does not involve radiation exposure, as a test to precisely evaluate the function of the UES. Material and methods Participants All subjects were patients with dysphagia. From June 2012 to October 2013, 266 patients were referred to the Swallowing Center in our hospital for an assessment of their swallowing function in an outpatient setting. All 266 patients were assessed with VFSS and VESS. In 52 patients, MVE was also performed to obtain precise information about the pharyngeal contraction and UES function. The inclusion criteria for this study were: (1) patients with dysphagia, (2) informed consent from the patient to undergo VFSS and MVE. The exclusion criteria were: (1) age less than 20 years, (2) current episode of pneumonia, and (3) patients with severe dementia. The study participants included 43 males and 9 females, with an age range of 36–97 years. Their primary diseases are described in Table I.
Table I. Patients’ characteristics. Characteristic
Value
Sex Male Female Average age, years (range)
43 9 73 (36–97)
Primary disease Cerebrovascular accident
14
Parkinson’s disease/syndrome
10
Aspiration pneumonia
7
Brain tumor
4
Unknown
3
Amyotrophic lateral sclerosis
1
Post thoracic surgery Others
1 12
Fourteen patients had had cerebrovascular accidents and the other patients had various other diseases. Informed consent was obtained from each patient for the evaluations and analysis and publication of their data. This study was carried out in Kyorin University Hospital Swallowing Center, Mitaka, Tokyo, Japan and was approved by the Research Ethics Committee of the university. Apparatus Mogram Stealth, a manometry and video synchronized recording and analyzing system (Star Medical Co., Tokyo, Japan) was utilized for MVE. The video endoscope system used was the VISERA Pro (Olympus Medical System Co., Tokyo, Japan), with an endoscopic diameter of 3.9 mm. The manometry catheter was 100 cm long and 2.6 mm in outer diameter (UniTip Katheter, Unisensor, Attikon, Switzerland), with four solid-state circumferential sensors, each 2 cm apart. The sensor sensitivity was 5 mV/V/mmHg (± 2%). Digital 12-bit samples were obtained via a GMMS pocket monitor (4th pocket monitor GMMS-400, Star Medical Co.), with a sampling frequency of 100 Hz, and were displayed in a display window. The system software program, Eight STAR for windows XP (Star Medical Co.) was used to generate the pressure waveforms, and the waveforms and endoscopic images were displayed on the same monitor (Figure 1). Procedure First, a videoendoscopic evaluation of swallowing was performed [8]. Next, a manometric catheter was
Mano-videoendoscopic swallowing study
189
CH-1 ±4
200.00 mHg -6.500
0.00
Sensor one
CH-2 ±3
200.00 mHg
Sensor one
1.000
Sensor two Sensor two
0.00 CH-3 ±2
200.00 mHg
Sensor three
-18.000
Sensor three
8.500
±1
CH-4
0.00 200.00 mHg
Sensor four
0.00 00:00:27.820
5s
10s
15s
20s
25s
30s
Figure 1. The waveforms and endoscopic image. Sensor three was located at the level of the pyriform sinus apex. Sensor four was kept in the upper esophageal sphincter.
inserted transnasally. The pressures were measured in the UES (sensor four) and at 2, 4, and 6 cm proximally, corresponding to the levels of the apex of the pyriform sinus (sensor three), upper pyriform sinus (sensor two), and tongue base (sensor one), respectively. During the procedure, an otolaryngologist held the endoscope with the left hand and operated the pressure catheter using the right hand. While the endoscope and pressure waveforms were monitored, the pressure sensors were placed and fixed. If the sensor was displaced, it was repositioned with fine adjustment. The assistant placed test food (a colored jelly) in the mouth of the subject. The subject was then asked to swallow 3 ml of colored jelly three times, and the resulting pressure waveforms were recorded. VFSS was performed within 1 week of MVE. In this test, the subject sat on a chair, and the image field was adjusted to include the entire oropharynx and upper esophagus. A coin (2.25 cm in diameter) was taped under the chin, and lateral videofluorography was performed using the coin as a reference. The test boluses administered were 3, 5, and 10 ml of nonionic, low-osmolar, iodinated contrast agent (Iopamidol). The subject swallowed the contrast medium as a single bolus on command. Fluoroscopic images, obtained at a rate of 30 frames per second, were displayed on separate monitors and recorded with a digital videocassette recorder (GV-HD700/1 Sony Co., Tokyo, Japan) onto a videocassette (Mini DV 60, Sony Co.). A video-timer (VTD-55D, For-A Co. Ltd, Tokyo, Japan) was used for the temporal analysis.
Analysis Since a high rate of agreement has already been shown between VESS and VFSS in terms of aspiration and hypopharyngeal residue [9], we focused on the comparisons between the manometric findings of UES relaxation and the fluorographic findings of UES opening in this study. Based on previous reports [10–12], we measured the resting pressure (mmHg), nadir (lowest) pressure (mmHg), pressure drop (mmHg), peak pressure of the C wave (mmHg), pressure rise (mmHg) in the UES, and relaxation time (ms) of the UES. The names used for the waves in the UES followed those in the report by McConnel [5]. The resting pressure of the UES was considered to be the continuous positive pressure during the resting period. The pressure drop indicated the gap between the resting pressure and the nadir of the UES pressure. The pressure rise indicated the gap between the nadir pressure and the peak pressure of the C (constrictor) wave. The duration of UES relaxation was the time between the peak time of the E (elevation) wave and the peak time of the C wave (Figure 2). Using lateral projection of the fluoroscopic image, two board-certified otolaryngologists evaluated the opening of the UES, grading the state of the UES opening as being good or poor. Thereafter, the parameters of waveforms in the UES were compared between the good and poor UES opening groups. Welch's t-test was used for the comparison between the two groups. A one-way analysis of variance was used for the statistical analysis of the variables. Values of p £ 0.05 were considered to be statistically significant.
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Table III. Logistic regression test.
E
Parameter D C
E Wave
0 mmHg
A
B
A receiver operating characteristic (ROC) analysis was performed to assess the sensitivity and specificity of the cut-off values for the manometric data for predicting the fluoroscopic opening of the UES. Results Using videofluorography, the UES opening was diagnosed as good in 34 patients and poor in 18 patients (Table II). No significant differences were observed between the two groups in terms of the age distribution, with the values being 73.7 ± 12.4 years (mean ± SD) in the good opening group and 71.7 ± 11.9 in the poor opening group (p = 0.318). The nadir, pressure drop, peak pressure, and pressure rise in the UES were significantly different between the two groups. The pressure drop was significantly
0.924
0.892–0.957
< 0.001
Pressure rise
0.995
0.990–1.000
0.077
Duration of relaxation
1.000
0.998–1.000
0.525
larger in the good opening group than in the poor opening group (44.1 ±11.5 mmHg and 28.6 ± 16.3 mmHg, respectively, p < 0.001). The peak pressure of the C wave and the pressure rise were both significantly larger in the good opening group than in the poor opening group (p = 0.002 and p < 0.001, respectively) (Table II). A stepwise logistic regression test revealed that the pressure drop was the most useful parameter predicting the fluorographic UES opening (Table III). A ROC analysis was performed to assess the sensitivity and specificity of the cut-off values for the pressure drop in predicting the fluorographic opening of the UES, and the cut-off level to anticipate good fluorographic opening of the UES was > 33.5 mmHg (specificity, 0.853; sensitivity, 0.759; AUC, 0.808) (Figure 3). Discussion A major finding of this study was that manometry with a videoendoscope could objectively and quantitatively 1.0
0.8
Parameter
0.6
0.269
3.4 ± 12.7
< 0.001
44.1 ± 11.5
28.6 ± 16.3
< 0.001
Peak pressure of C wave (mmHg)
153.8 ± 88.3
110.4 ± 70.9
0.002
Pressure rise in UES (mmHg)
164.3 ± 86.9
108.5 ± 71.9
< 0.001
Duration of UES relaxation (ms)
1057 ± 296
Pressure drop in UES (mmHg)
–10.1 ± 7.6
33.500 (0.853, 0.759) Sensitivity
Good opening of Poor opening of p value UES: 34 subjects UES: 18 patients (102 swallows) (54 swallows) 31.5 ± 16.0
Nadir in UES (mmHg)
p value
Pressure drop
Table II. Correlation between fluorographic upper esophageal sphincter (UES) opening and manometric parameters of UES function.
33.9 ± 11.4
95% CI
CI, confidence interval; OR, odds ratio.
Figure 2. Manometric parameters. (A) Resting pressure (the continuous positive pressure during the resting period) in the upper esophageal sphincter (UES). (B) Pressure drop (the gap between the resting pressure and the nadir of the UES pressure). (C) Peak pressure of the C wave. (D) Pressure rise (the gap between the nadir pressure and the peak pressure of the C wave). (E) Duration of relaxation (duration between the peak time of the E wave and the peak time of the C wave).
UES resting pressure (mmHg)
OR
0.4
0.2
0.0 1.0
0.8
0.6
0.4
0.2
0.0
Specificity 955 ± 328
0.050
Values are means ± standard deviation. MVE, manovideoendoscopy; VFSS, videofluorographic swallowing study.
Figure 3. Receiver operating characteristic (ROC) curve and the sensitivity and specificity of the cut-off values for the pressure drop in predicting the fluorographic opening of the upper esophageal sphincter (UES).
Mano-videoendoscopic swallowing study clarify the UES function, which is not possible with VESS. In this study, we were able to position the lowest sensor in the UES, which is not visible nasoendoscopically, by adopting two indicators. The first was to hold the third sensor at the apex of the pyriform sinus, and the second was to confirm the characteristic pressure waveform of the UES (Figure 2). In 2007, Butler et al. reported using a similar technique to perform manometry with a transnasally inserted catheter under endoscopic observation when performing VESS [13]. However, if the outer diameters of the solid-state sensors and the catheter are large, it is possible that patients will have a foreign body sensation in the pharynx, which will result in a change in the swallowing dynamics from normal. To address this, Butler et al. investigated the effects of a transnasally inserted manometric catheter (outer diameter of 2.1 mm) on the swallowing dynamics using fluorography, and they reported that there were no effects on the swallowing movement [14]. Because the catheter we used had an outer diameter of 2.6 mm, we think that there were limited effects on the swallowing dynamics. The magnitude of the UES pressure is directly related to the size of recording assembly [15]. Previous studies have shown that increases in the manometric assembly diameter caused significant increases in swallowing pressure and resting pressure [12,15]. A thinner catheter may be less invasive, which may therefore contribute to obtaining more physiological measurements [12]. In general, manometry records sphincter relaxation, whereas X-ray imaging records sphincter opening. These two phenomena are related, but are distinct events [16]. The cricopharyngeal muscle relaxes during elevation, which also opens the UES. Both laryngeal elevation and cricopharyngeal relaxation are essential for the normal opening of the UES for bolus passage [5]. An earlier study of manofluorographic assessment revealed that as the larynx accelerates during elevation, it moves anteriorly, pulling the cricoid lamina away from the posterior pharyngeal wall, thus opening the UES [5]. With maximal opening, an additional negative pressure notch is developed. This negative pressure occurs immediately before bolus arrival [5]. In this study, the magnitude of the pressure drop was related to the fluorographic UES opening. The negative pressure and the magnitude of the pressure drop may be key parameters of the UES relaxation function. More recently, there have been some reports of monitoring the swallowing pressure from the pharynx to the stomach and plotting the pressure topography
191
using high-resolution manometry (HRM). A previous study using HRM provided a more comprehensive picture of how the bolus volume affects the swallowing physiology [10]. Ghosh et al. demonstrated that the lowest (nadir) pressure in the UES was 5.42 ± 4.53 mmHg in normal controls [17], and they rarely saw negative UES pressures, as have been reported [5]. The manometric assembly of the HRM system usually has an outer diameter of 4.1 or 4.2 mm, 36 circumferential sensors, with a fidelity of 2 mmHg, and the sampling rate is 35–50 Hz. Because of the low sampling frequency of HRM, it may be difficult to grasp the steep pressure change in the UES and to see negative UES pressures. Therefore, in the present study, we first assumed that the duration of UES relaxation might be an indicator of whether there was good or poor fluorographic UES opening. According to previous reports [10–12], the duration of the UES relaxation was defined as the time lapse between the two pressure (E wave and C wave) peaks for bolus passage. There was no statistically significant difference in our two patient groups, but the poor UES opening group tended to have a shorter duration of UES relaxation than the good opening group. A previous study reported similar results (0.94 ± 0.18 s in normal controls and 0.85 ± 0.28 s in dysphagic patients) [11]. The duration of UES relaxation may therefore be one of the indicators of UES dysfunction. The limitations of this study include its retrospective nature, comparing the manometric and fluoroscopic findings of the patients with dysphagia. This study showed that the findings of fluorographic UES opening were significantly associated with the pressure drop in the UES. Because this was not a prospective study, we could not actually predict the fluorographic UES opening based on the results of the manometric findings of UES. Future prospective studies to estimate the UES opening based on the pressure data would be beneficial. Another problem was that the swallow-induced orad excursion of the UES carried the sphincter proximal to the recording sensor, so that the sensor ‘drops’ into the cervical esophagus [16]. The subjects needed to perform dry swallows several times to position the sensor at the appropriate position and to confirm the characteristic pressure waveforms of the UES. This may be a limitation of using a small number of sensors [10], but it was not difficult to capture the relevant pressure data. In this study, all subjects were patients with dysphagia, and we did not collect data from normal controls. Previous studies have evaluated the resting and nadir pressures in normal subjects; however, there are no previous studies assessing both the
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resting and nadir pressures. Matsubara et al. showed the resting pressure in normal subjects (n = 36) to be 44 ± 13 mmHg [12], and Hoffman et al. reported that the nadir (minimum) pressure in normal subjects (n = 12) is –4 ± 7 mmHg [10]. Because these findings do not reflect pressure changes in the same individual, it is not appropriate to compare them with our data. Nevertheless, the mean difference in these previous studies was 48 mmHg. In the current study, the mean pressure drop in the patients in the good UES opening group (34 patients, 102 swallows) was 44 mmHg, a similar value. Further investigations regarding the standardization of these parameters in normal subjects are needed. Manometric parameters can be affected by age in normal subjects. Using Spearman’s rank correlation coefficient, we evaluated the correlation between the pressure drop and age in the good UES opening group (34 patients, 102 swallows) and found no statistically significant correlations (r = –0.105, p = 0.284). Further investigations regarding the influence of age on these parameters in normal subjects are required. A novel parameter developed in this study was the pressure drop. The manometric pressure drop in the UES can be a robust predictor of the fluorographic UES opening. Because this parameter is relatively easy to calculate, it can easily be applied in the outpatient clinic. If it is possible to predict whether a patient will have good or poor fluorographic opening of the UES based on the data provided by MVE, it might be possible to omit videofluorography for the purpose of examining UES function. Conclusion By performing manometry in addition to standard VESS techniques, it is possible to supplement the functional evaluations of UES function, thus overcoming the drawbacks of VESS. MVE can be used in place of VFSS as a test of UES function; with this technique, detailed information on the swallowing function can be obtained. When we analyze the UES function with MVE, the pressure drop can be a robust predictor of fluorographic UES opening. Declaration of interest: The authors report no financial and material support and no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
References [1] Langmore SE, Schatz K, Olsen N. Fiberoptic endoscopic examination of swallowing safety: a new procedure. Dysphagia 1988;2:216–19. [2] Langmore SE, Schatz K, Olsen N. Endoscopic and videofluoroscopic evaluations of swallowing and aspiration. Ann Otol Rhinol Laryngol 1991;100:678–81. [3] Bastian RW. The videoendoscopic swallowing study: an alternative and partner to the videofluoroscopic swallowing study. Dysphagia 1993;8:359–67. [4] Matsumura Y, Karaho T, Tanabe T, Kitahara S. [Manofluorographic analysis of bolus volume effect in normal swallowing]. J Jpn Bronchoesophagol Soc 2006;57:351–62; in Japanese. [5] McConnelFM.Analysisofpressuregenerationandbolustransit during pharyngeal swallowing. Laryngoscope 1988;98:71–8. [6] Kahrilas PJ, Dodds WJ, Dent J, Logemann JA, Shaker R. Upper esophageal sphincter function during deglutition. Gastroenterology 1988;95:52–62. [7] Karaho T, Nakajima J, Kitagawa Y, Sato T, Kohno N. Mano-videoendoscopic evaluation of dysphagia (abstract). Dysphagia 2009;24:458. [8] Langmore SE, Aviv JE. Endoscopic procedure to evaluate oropharyngeal swallowing. In Langmore SE, editor. Endoscopic evaluation and treatment of swallowing disorders. Thieme. New York, NY: 2001. p 73–100. [9] Aviv JE. Prospective, randomized outcome study of endoscopy versus modified barium swallow in patients with dysphagia. Laryngoscope 2000;110:563–74. [10] Hoffman MR, Ciucci MR, Mielens JD, Jiang JJ, McCulloch TM. Pharyngeal swallow adaptations to bolus volume measured with high-resolution manometry. Laryngoscope 2010;120:2367–73. [11] Mielens JD, Hoffman MR, Ciucci MR, McCulloch TM, Jiang JJ. Application of classification models to pharyngeal high-resolution manometry. J Speech Lang Hear Res 2012; 55:892–902. [12] Matsubara K, Kumai Y, Samejima Y, Yumoto E. Swallowing pressure and pressure profiles in young healthy adults. Laryngoscope 2014;124:711–17. [13] Butler SG, Stuart A, Castell D, Russell G, Koch K, Kemp S. Effects of age, gender, bolus volume, condition, viscosity, and volume on pharyngeal and upper esophageal sphincter pressure and temporal measurements during swallowing (abstract). Dysphagia 2007;22:367. [14] Butler SG, Rees C, Markley L, Stuart A. Effects of manometric catheter on flexible endoscopic evaluation of swallowing (VEES) in healthy older adults (abstract). Dysphagia 2008;23:446. [15] Lyndon SB. The effect of manometric assembly diameter on intraluminal esophageal pressure recording. Am J Dig Dis 1975;20:968–70. [16] Dodds WJ, Kahrilas PJ, Dent J, Hogan WJ. Consideration about pharyngeal manometry. Dysphagia 1987;1:209–14. [17] Ghosh SK, Pandolfino JE, Zhang Q, Jarosz A, Kahrilas PJ. Deglutitive upper esophageal sphincter relaxation: a study of 75 volunteer subjects using solid-state high-resolution manometry. Am J Physiol Gastrointest Liver Physiol 2006; 291:G525–31.
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ORIGINAL ARTICLE
Can mano-videoendoscopy substitute for videofluorography in evaluation of upper esophageal sphincter function?
TAKEHIRO KARAHO1,2, TETSUYA SATOH1,2, JUNKO NAKAJIMA2,3, TAKESHI NAKAYAMA2,4 & NAOYUKI KOHNO1 PRESENTED AT THE 36TH ANNUAL CONFERENCE OF THE SOCIETY OF SWALLOWING AND DYSPHAGIA OF JAPAN, KYOTO, MARCH 1–2, 2013. 1
Department of Otolaryngology Head and Neck Surgery, Kyorin University, School of Medicine, Mitaka, Tokyo, 2Kyorin University Hospital Swallowing Center, Mitaka, Tokyo, 3Department of Oral and Maxillofacial Surgery, National Defense Medical College, Tokorozawa, Saitama and 4Japan Welfare Education College, Shinjuku, Tokyo, Japan
Abstract Conclusions: Mano-videoendoscopy (MVE), a manometry technique with endoscopic confirmation of the pressure catheter, can supplement the information on upper esophageal sphincter (UES) function, and overcomes the drawbacks of videoendoscopic swallowing study (VESS). Objectives: This study aimed to investigate the possibility of replacing videofluorographic swallowing study (VFSS) with MVE, as a test to precisely evaluate UES function. Methods: Data from 52 patients with dysphagia were retrospectively reviewed. All patients underwent both MVE and VFSS for evaluation of dysphagia. The manometry was performed with a transnasally inserted catheter (2.6 mm outer diameter and four pressure sensors) under endoscopic observation. The sensors were kept at the tongue base, upper pyriform sinus, apex of pyriform sinus, and UES. We statistically compared the manometric parameters of UES relaxation with fluorographic UES opening. Results: Fluorographic UES opening was diagnosed as good in 34 patients and poor in 18 patients. The nadir pressure, pressure drop, and pressure rise in the UES had significant correlation on the fluorographic UES opening. Stepwise logistic regression test revealed that pressure drop, the gap between the resting pressure and the nadir of UES pressure, was a robust parameter for predicting fluorographic UES opening, and the cut-off level to anticipate good fluorographic opening was ‡ 33.5 mmHg (specificity, 0.853; sensitivity, 0.759)
Keywords: swallowing study, fluorography, dysphagia
Introduction Videoendoscopic swallowing studies (VESS) have become the standard method for examining the swallowing function in patients with dysphagia, because the procedure is relatively non-invasive and can even be performed at the patient’s bedside. Initially, it was performed mostly in patients who could not be adequately examined with videofluorographic swallowing studies (VFSS), which is viewed as the gold standard of swallowing function tests [1]. However, due to their portability and convenient use,
endoscopic examinations are now performed at some institutions as a test of swallowing function in place of videofluorography [2,3]. In institutions where both examinations can be performed, VESS and VFSS are generally used complementarily [3]. Compared with videofluorography, endoscopic examination has the disadvantages of not allowing visualization of the oral and esophageal stages of swallowing, the pharyngeal contraction cannot be objectively evaluated, and the opening (relaxation) of the upper esophageal sphincter (UES) cannot be observed [3]. The opening of the UES is a
Correspondence: Takehiro Karaho, Department of Otolaryngology Head and Neck Surgery, Kyorin University, School of Medicine, 6-20-2, Shinkawa, Mitaka, Tokyo, 181-8611, Japan. Tel: +81 422 47 5511. E-mail: [email protected]
(Received 19 July 2014; accepted 4 September 2014) ISSN 0001-6489 print/ISSN 1651-2251 online 2015 Informa Healthcare DOI: 10.3109/00016489.2014.969384
188
T. Karaho et al.
phenomenon that occurs as a result of the relaxation of the cricopharyngeal muscle and laryngeal elevation, although the opening and relaxation of the sphincter do not occur at exactly the same time [4,5]. Information about the presence or absence of UES opening (relaxation) is especially important, as it affects the subsequent treatment strategy, and examinations that cannot evaluate this are inadequate as examinations of the swallowing function. Manometry, which is used to measure the pressure in the pharynx and esophagus during swallowing, enables the observation of the swallowing pressure, which indicates the force of the propulsion of a bolus of food at the level of the base of the tongue, and the relaxation status of the UES [4–6]. However, pressure waveforms differ depending on the positions in which the solid-state sensors are placed. In patients with pharyngeal dysphagia, the pressure catheter is sometimes accidentally inserted into the larynx rather than the esophagus. Since it is therefore advisable to confirm the position of the solid-state sensors during examination, videofluorography is usually performed simultaneously with manometry [4,5]. In such cases, however, the radiation exposure is a problem. Mano-videoendoscopy (MVE) is a technique used to obtain additional manometric information, for example, information about pharyngeal contraction and UES relaxation, after a routine VESS examination [7]. This procedure may reduce the VFSS for the purpose of analyzing the UES function. The aim of the present study was to investigate the possibility of replacing VFSS with MVE, which does not involve radiation exposure, as a test to precisely evaluate the function of the UES. Material and methods Participants All subjects were patients with dysphagia. From June 2012 to October 2013, 266 patients were referred to the Swallowing Center in our hospital for an assessment of their swallowing function in an outpatient setting. All 266 patients were assessed with VFSS and VESS. In 52 patients, MVE was also performed to obtain precise information about the pharyngeal contraction and UES function. The inclusion criteria for this study were: (1) patients with dysphagia, (2) informed consent from the patient to undergo VFSS and MVE. The exclusion criteria were: (1) age less than 20 years, (2) current episode of pneumonia, and (3) patients with severe dementia. The study participants included 43 males and 9 females, with an age range of 36–97 years. Their primary diseases are described in Table I.
Table I. Patients’ characteristics. Characteristic
Value
Sex Male Female Average age, years (range)
43 9 73 (36–97)
Primary disease Cerebrovascular accident
14
Parkinson’s disease/syndrome
10
Aspiration pneumonia
7
Brain tumor
4
Unknown
3
Amyotrophic lateral sclerosis
1
Post thoracic surgery Others
1 12
Fourteen patients had had cerebrovascular accidents and the other patients had various other diseases. Informed consent was obtained from each patient for the evaluations and analysis and publication of their data. This study was carried out in Kyorin University Hospital Swallowing Center, Mitaka, Tokyo, Japan and was approved by the Research Ethics Committee of the university. Apparatus Mogram Stealth, a manometry and video synchronized recording and analyzing system (Star Medical Co., Tokyo, Japan) was utilized for MVE. The video endoscope system used was the VISERA Pro (Olympus Medical System Co., Tokyo, Japan), with an endoscopic diameter of 3.9 mm. The manometry catheter was 100 cm long and 2.6 mm in outer diameter (UniTip Katheter, Unisensor, Attikon, Switzerland), with four solid-state circumferential sensors, each 2 cm apart. The sensor sensitivity was 5 mV/V/mmHg (± 2%). Digital 12-bit samples were obtained via a GMMS pocket monitor (4th pocket monitor GMMS-400, Star Medical Co.), with a sampling frequency of 100 Hz, and were displayed in a display window. The system software program, Eight STAR for windows XP (Star Medical Co.) was used to generate the pressure waveforms, and the waveforms and endoscopic images were displayed on the same monitor (Figure 1). Procedure First, a videoendoscopic evaluation of swallowing was performed [8]. Next, a manometric catheter was
Mano-videoendoscopic swallowing study
189
CH-1 ±4
200.00 mHg -6.500
0.00
Sensor one
CH-2 ±3
200.00 mHg
Sensor one
1.000
Sensor two Sensor two
0.00 CH-3 ±2
200.00 mHg
Sensor three
-18.000
Sensor three
8.500
±1
CH-4
0.00 200.00 mHg
Sensor four
0.00 00:00:27.820
5s
10s
15s
20s
25s
30s
Figure 1. The waveforms and endoscopic image. Sensor three was located at the level of the pyriform sinus apex. Sensor four was kept in the upper esophageal sphincter.
inserted transnasally. The pressures were measured in the UES (sensor four) and at 2, 4, and 6 cm proximally, corresponding to the levels of the apex of the pyriform sinus (sensor three), upper pyriform sinus (sensor two), and tongue base (sensor one), respectively. During the procedure, an otolaryngologist held the endoscope with the left hand and operated the pressure catheter using the right hand. While the endoscope and pressure waveforms were monitored, the pressure sensors were placed and fixed. If the sensor was displaced, it was repositioned with fine adjustment. The assistant placed test food (a colored jelly) in the mouth of the subject. The subject was then asked to swallow 3 ml of colored jelly three times, and the resulting pressure waveforms were recorded. VFSS was performed within 1 week of MVE. In this test, the subject sat on a chair, and the image field was adjusted to include the entire oropharynx and upper esophagus. A coin (2.25 cm in diameter) was taped under the chin, and lateral videofluorography was performed using the coin as a reference. The test boluses administered were 3, 5, and 10 ml of nonionic, low-osmolar, iodinated contrast agent (Iopamidol). The subject swallowed the contrast medium as a single bolus on command. Fluoroscopic images, obtained at a rate of 30 frames per second, were displayed on separate monitors and recorded with a digital videocassette recorder (GV-HD700/1 Sony Co., Tokyo, Japan) onto a videocassette (Mini DV 60, Sony Co.). A video-timer (VTD-55D, For-A Co. Ltd, Tokyo, Japan) was used for the temporal analysis.
Analysis Since a high rate of agreement has already been shown between VESS and VFSS in terms of aspiration and hypopharyngeal residue [9], we focused on the comparisons between the manometric findings of UES relaxation and the fluorographic findings of UES opening in this study. Based on previous reports [10–12], we measured the resting pressure (mmHg), nadir (lowest) pressure (mmHg), pressure drop (mmHg), peak pressure of the C wave (mmHg), pressure rise (mmHg) in the UES, and relaxation time (ms) of the UES. The names used for the waves in the UES followed those in the report by McConnel [5]. The resting pressure of the UES was considered to be the continuous positive pressure during the resting period. The pressure drop indicated the gap between the resting pressure and the nadir of the UES pressure. The pressure rise indicated the gap between the nadir pressure and the peak pressure of the C (constrictor) wave. The duration of UES relaxation was the time between the peak time of the E (elevation) wave and the peak time of the C wave (Figure 2). Using lateral projection of the fluoroscopic image, two board-certified otolaryngologists evaluated the opening of the UES, grading the state of the UES opening as being good or poor. Thereafter, the parameters of waveforms in the UES were compared between the good and poor UES opening groups. Welch's t-test was used for the comparison between the two groups. A one-way analysis of variance was used for the statistical analysis of the variables. Values of p £ 0.05 were considered to be statistically significant.
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T. Karaho et al. C Wave
Table III. Logistic regression test.
E
Parameter D C
E Wave
0 mmHg
A
B
A receiver operating characteristic (ROC) analysis was performed to assess the sensitivity and specificity of the cut-off values for the manometric data for predicting the fluoroscopic opening of the UES. Results Using videofluorography, the UES opening was diagnosed as good in 34 patients and poor in 18 patients (Table II). No significant differences were observed between the two groups in terms of the age distribution, with the values being 73.7 ± 12.4 years (mean ± SD) in the good opening group and 71.7 ± 11.9 in the poor opening group (p = 0.318). The nadir, pressure drop, peak pressure, and pressure rise in the UES were significantly different between the two groups. The pressure drop was significantly
0.924
0.892–0.957
< 0.001
Pressure rise
0.995
0.990–1.000
0.077
Duration of relaxation
1.000
0.998–1.000
0.525
larger in the good opening group than in the poor opening group (44.1 ±11.5 mmHg and 28.6 ± 16.3 mmHg, respectively, p < 0.001). The peak pressure of the C wave and the pressure rise were both significantly larger in the good opening group than in the poor opening group (p = 0.002 and p < 0.001, respectively) (Table II). A stepwise logistic regression test revealed that the pressure drop was the most useful parameter predicting the fluorographic UES opening (Table III). A ROC analysis was performed to assess the sensitivity and specificity of the cut-off values for the pressure drop in predicting the fluorographic opening of the UES, and the cut-off level to anticipate good fluorographic opening of the UES was > 33.5 mmHg (specificity, 0.853; sensitivity, 0.759; AUC, 0.808) (Figure 3). Discussion A major finding of this study was that manometry with a videoendoscope could objectively and quantitatively 1.0
0.8
Parameter
0.6
0.269
3.4 ± 12.7
< 0.001
44.1 ± 11.5
28.6 ± 16.3
< 0.001
Peak pressure of C wave (mmHg)
153.8 ± 88.3
110.4 ± 70.9
0.002
Pressure rise in UES (mmHg)
164.3 ± 86.9
108.5 ± 71.9
< 0.001
Duration of UES relaxation (ms)
1057 ± 296
Pressure drop in UES (mmHg)
–10.1 ± 7.6
33.500 (0.853, 0.759) Sensitivity
Good opening of Poor opening of p value UES: 34 subjects UES: 18 patients (102 swallows) (54 swallows) 31.5 ± 16.0
Nadir in UES (mmHg)
p value
Pressure drop
Table II. Correlation between fluorographic upper esophageal sphincter (UES) opening and manometric parameters of UES function.
33.9 ± 11.4
95% CI
CI, confidence interval; OR, odds ratio.
Figure 2. Manometric parameters. (A) Resting pressure (the continuous positive pressure during the resting period) in the upper esophageal sphincter (UES). (B) Pressure drop (the gap between the resting pressure and the nadir of the UES pressure). (C) Peak pressure of the C wave. (D) Pressure rise (the gap between the nadir pressure and the peak pressure of the C wave). (E) Duration of relaxation (duration between the peak time of the E wave and the peak time of the C wave).
UES resting pressure (mmHg)
OR
0.4
0.2
0.0 1.0
0.8
0.6
0.4
0.2
0.0
Specificity 955 ± 328
0.050
Values are means ± standard deviation. MVE, manovideoendoscopy; VFSS, videofluorographic swallowing study.
Figure 3. Receiver operating characteristic (ROC) curve and the sensitivity and specificity of the cut-off values for the pressure drop in predicting the fluorographic opening of the upper esophageal sphincter (UES).
Mano-videoendoscopic swallowing study clarify the UES function, which is not possible with VESS. In this study, we were able to position the lowest sensor in the UES, which is not visible nasoendoscopically, by adopting two indicators. The first was to hold the third sensor at the apex of the pyriform sinus, and the second was to confirm the characteristic pressure waveform of the UES (Figure 2). In 2007, Butler et al. reported using a similar technique to perform manometry with a transnasally inserted catheter under endoscopic observation when performing VESS [13]. However, if the outer diameters of the solid-state sensors and the catheter are large, it is possible that patients will have a foreign body sensation in the pharynx, which will result in a change in the swallowing dynamics from normal. To address this, Butler et al. investigated the effects of a transnasally inserted manometric catheter (outer diameter of 2.1 mm) on the swallowing dynamics using fluorography, and they reported that there were no effects on the swallowing movement [14]. Because the catheter we used had an outer diameter of 2.6 mm, we think that there were limited effects on the swallowing dynamics. The magnitude of the UES pressure is directly related to the size of recording assembly [15]. Previous studies have shown that increases in the manometric assembly diameter caused significant increases in swallowing pressure and resting pressure [12,15]. A thinner catheter may be less invasive, which may therefore contribute to obtaining more physiological measurements [12]. In general, manometry records sphincter relaxation, whereas X-ray imaging records sphincter opening. These two phenomena are related, but are distinct events [16]. The cricopharyngeal muscle relaxes during elevation, which also opens the UES. Both laryngeal elevation and cricopharyngeal relaxation are essential for the normal opening of the UES for bolus passage [5]. An earlier study of manofluorographic assessment revealed that as the larynx accelerates during elevation, it moves anteriorly, pulling the cricoid lamina away from the posterior pharyngeal wall, thus opening the UES [5]. With maximal opening, an additional negative pressure notch is developed. This negative pressure occurs immediately before bolus arrival [5]. In this study, the magnitude of the pressure drop was related to the fluorographic UES opening. The negative pressure and the magnitude of the pressure drop may be key parameters of the UES relaxation function. More recently, there have been some reports of monitoring the swallowing pressure from the pharynx to the stomach and plotting the pressure topography
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using high-resolution manometry (HRM). A previous study using HRM provided a more comprehensive picture of how the bolus volume affects the swallowing physiology [10]. Ghosh et al. demonstrated that the lowest (nadir) pressure in the UES was 5.42 ± 4.53 mmHg in normal controls [17], and they rarely saw negative UES pressures, as have been reported [5]. The manometric assembly of the HRM system usually has an outer diameter of 4.1 or 4.2 mm, 36 circumferential sensors, with a fidelity of 2 mmHg, and the sampling rate is 35–50 Hz. Because of the low sampling frequency of HRM, it may be difficult to grasp the steep pressure change in the UES and to see negative UES pressures. Therefore, in the present study, we first assumed that the duration of UES relaxation might be an indicator of whether there was good or poor fluorographic UES opening. According to previous reports [10–12], the duration of the UES relaxation was defined as the time lapse between the two pressure (E wave and C wave) peaks for bolus passage. There was no statistically significant difference in our two patient groups, but the poor UES opening group tended to have a shorter duration of UES relaxation than the good opening group. A previous study reported similar results (0.94 ± 0.18 s in normal controls and 0.85 ± 0.28 s in dysphagic patients) [11]. The duration of UES relaxation may therefore be one of the indicators of UES dysfunction. The limitations of this study include its retrospective nature, comparing the manometric and fluoroscopic findings of the patients with dysphagia. This study showed that the findings of fluorographic UES opening were significantly associated with the pressure drop in the UES. Because this was not a prospective study, we could not actually predict the fluorographic UES opening based on the results of the manometric findings of UES. Future prospective studies to estimate the UES opening based on the pressure data would be beneficial. Another problem was that the swallow-induced orad excursion of the UES carried the sphincter proximal to the recording sensor, so that the sensor ‘drops’ into the cervical esophagus [16]. The subjects needed to perform dry swallows several times to position the sensor at the appropriate position and to confirm the characteristic pressure waveforms of the UES. This may be a limitation of using a small number of sensors [10], but it was not difficult to capture the relevant pressure data. In this study, all subjects were patients with dysphagia, and we did not collect data from normal controls. Previous studies have evaluated the resting and nadir pressures in normal subjects; however, there are no previous studies assessing both the
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resting and nadir pressures. Matsubara et al. showed the resting pressure in normal subjects (n = 36) to be 44 ± 13 mmHg [12], and Hoffman et al. reported that the nadir (minimum) pressure in normal subjects (n = 12) is –4 ± 7 mmHg [10]. Because these findings do not reflect pressure changes in the same individual, it is not appropriate to compare them with our data. Nevertheless, the mean difference in these previous studies was 48 mmHg. In the current study, the mean pressure drop in the patients in the good UES opening group (34 patients, 102 swallows) was 44 mmHg, a similar value. Further investigations regarding the standardization of these parameters in normal subjects are needed. Manometric parameters can be affected by age in normal subjects. Using Spearman’s rank correlation coefficient, we evaluated the correlation between the pressure drop and age in the good UES opening group (34 patients, 102 swallows) and found no statistically significant correlations (r = –0.105, p = 0.284). Further investigations regarding the influence of age on these parameters in normal subjects are required. A novel parameter developed in this study was the pressure drop. The manometric pressure drop in the UES can be a robust predictor of the fluorographic UES opening. Because this parameter is relatively easy to calculate, it can easily be applied in the outpatient clinic. If it is possible to predict whether a patient will have good or poor fluorographic opening of the UES based on the data provided by MVE, it might be possible to omit videofluorography for the purpose of examining UES function. Conclusion By performing manometry in addition to standard VESS techniques, it is possible to supplement the functional evaluations of UES function, thus overcoming the drawbacks of VESS. MVE can be used in place of VFSS as a test of UES function; with this technique, detailed information on the swallowing function can be obtained. When we analyze the UES function with MVE, the pressure drop can be a robust predictor of fluorographic UES opening. Declaration of interest: The authors report no financial and material support and no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
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