effect of bolus volume on pharyngeal swallowing assessed by high-resolution manometry

6
Effect of bolus volume on pharyngeal swallowing assessed by high-resolution manometry , ☆☆ ,Tuo Lin a,1 , Guangqing Xu b,1 , Zulin Dou a , Yue Lan a, , Fan Yu a , Lisheng Jiang a a Department of Rehabilitation Medicine, The Third Afliated Hospital, Sun Yat-sen University, Guangzhou, China b Department of Rehabilitation Medicine, The First Afliated Hospital, Sun Yat-sen University, Guangzhou, China HIGHLIGHTS High-resolution manometry can detect the effect of volume on pharyngeal swallowing. Increase in bolus volume increases UES residual pressure and UES relaxation duration. Maximum preopening and postclosure UES pressures are not affected by bolus volume. Bolus volume has no effect on the hypopharynx. abstract article info Article history: Received 28 August 2013 Received in revised form 15 January 2014 Accepted 26 January 2014 Available online 8 February 2014 Keywords: Bolus volume Deglutition High-resolution manometry Swallowing physiology Objective: Solid-state high-resolution manometry (HRM) is fast becoming the gold standard for studying pharyngeal and esophageal motility. However, very few studies have ever evaluated the effect of bolus volume on the physiology of swallowing using HRM. We aimed to determine the effect of bolus volume on pressure, duration and velocity of the hypopharynx as well as the upper esophageal sphincter during pharyngeal swallowing using HRM. Methods: Thirty-four healthy subjects completed nine swallows (3 ml, 5 ml and 10 ml of water, thick liquid, and paste, respectively) in the natural sitting position. Pressure and duration measurements were acquired from the hypopharynx and upper esophageal sphincter (UES) using HRM. The UES residual pressure, UES relaxation duration, maximum preopening UES pressure, maximum postclosure UES pressure, maximum hypopharyngeal pressure, maximum hypopharyngeal pressure rise rate and hypopharyngeal pressure duration were analyzed across bolus volumes using repeated measures of one-way analysis of variance. Results: A signicant increase in UES residual pressure associated with increased bolus volume during water and paste swallowing was observed. Furthermore, UES relaxation duration was signicantly increased with increasing in bolus volume for all three material swallows. No signicant volume effects were found on the hypopharynx. Conclusions: In summary, bolus volume has a signicant effect on the residual pressure and relaxation duration, but no effect on maximum preopening pressure or maximum postclosure pressure of the UES. Maximum hypopharyngeal pressure, maximum hypopharyngeal pressure rise rate and pressure duration were also not affected by bolus volume. Consideration of these variables is paramount in understanding normal and patholog- ical swallowing. © 2014 Elsevier Inc. All rights reserved. 1. Introduction Bolus volume is an important modulator of the biomechanical events that occur during oropharyngeal swallowing [1]. In the case of varied volume bolus swallows, volume accommodation guarantees the safety and efcacy of swallowing. While patients with neurologically impaired dysphagia may face the risk of penetration and aspiration with increase in bolus volume, decrease in bolus volume beyond a certain extent may not trigger the automatic swallowing reex [2]. Therefore, alterations in bolus volume can bring about changes in swallowing physiology in ways that can compensate for or exacerbate decits. Volume modication in Physiology & Behavior 128 (2014) 4651 This work was completed at the University of Sun Yat-sen, China. ☆☆ Funding: This research was supported by grants 81101460 and 81371441 from the National Science Foundation of China, grant 2012J5100022 from the Guangzhou Municipal Science and Technology Program and grant 12ykpy38 from the Fundamental Research Funds for the Central Universities. Disclosure: No competing interests declared. Corresponding author. Tel.: +86 18988991916. E-mail address: [email protected] (Y. Lan). 1 These authors contributed equally to this work. 0031-9384/$ see front matter © 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.physbeh.2014.01.030 Contents lists available at ScienceDirect Physiology & Behavior journal homepage: www.elsevier.com/locate/phb

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Physiology & Behavior 128 (2014) 46–51

Contents lists available at ScienceDirect

Physiology & Behavior

j ourna l homepage: www.e lsev ie r .com/ locate /phb

Effect of bolus volume on pharyngeal swallowing assessed byhigh-resolution manometry☆,☆☆,★

Tuo Lin a,1, Guangqing Xu b,1, Zulin Dou a, Yue Lan a,⁎, Fan Yu a, Lisheng Jiang a

a Department of Rehabilitation Medicine, The Third Affiliated Hospital, Sun Yat-sen University, Guangzhou, Chinab Department of Rehabilitation Medicine, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China

H I G H L I G H T S

• High-resolution manometry can detect the effect of volume on pharyngeal swallowing.• Increase in bolus volume increases UES residual pressure and UES relaxation duration.• Maximum preopening and postclosure UES pressures are not affected by bolus volume.• Bolus volume has no effect on the hypopharynx.

☆ This work was completed at the University of Sun Y☆☆ Funding: This research was supported by grants 811National Science Foundation of China, grant 2012J5Municipal Science and Technology Program and grant 12Research Funds for the Central Universities.★ Disclosure: No competing interests declared.⁎ Corresponding author. Tel.: +86 18988991916.

E-mail address: [email protected] (Y. Lan).1 These authors contributed equally to this work.

0031-9384/$ – see front matter © 2014 Elsevier Inc. All rihttp://dx.doi.org/10.1016/j.physbeh.2014.01.030

a b s t r a c t

a r t i c l e i n f o

Article history:

Received 28 August 2013Received in revised form 15 January 2014Accepted 26 January 2014Available online 8 February 2014

Keywords:Bolus volumeDeglutitionHigh-resolution manometrySwallowing physiology

Objective: Solid-state high-resolution manometry (HRM) is fast becoming the gold standard for studyingpharyngeal and esophageal motility. However, very few studies have ever evaluated the effect of bolus volumeon the physiology of swallowing using HRM. We aimed to determine the effect of bolus volume on pressure,duration and velocity of the hypopharynx as well as the upper esophageal sphincter during pharyngealswallowing using HRM.Methods: Thirty-four healthy subjects completed nine swallows (3ml, 5 ml and 10ml of water, thick liquid, andpaste, respectively) in the natural sitting position. Pressure and duration measurements were acquired from thehypopharynx and upper esophageal sphincter (UES) using HRM. The UES residual pressure, UES relaxationduration, maximum preopening UES pressure, maximum postclosure UES pressure, maximum hypopharyngealpressure, maximum hypopharyngeal pressure rise rate and hypopharyngeal pressure duration were analyzed

across bolus volumes using repeated measures of one-way analysis of variance.Results: A significant increase in UES residual pressure associated with increased bolus volume during waterand paste swallowing was observed. Furthermore, UES relaxation duration was significantly increased withincreasing in bolus volume for all three material swallows. No significant volume effects were found on thehypopharynx.Conclusions: In summary, bolus volume has a significant effect on the residual pressure and relaxation duration,but no effect on maximum preopening pressure or maximum postclosure pressure of the UES. Maximumhypopharyngeal pressure, maximum hypopharyngeal pressure rise rate and pressure duration were also notaffected by bolus volume. Consideration of these variables is paramount in understanding normal and patholog-ical swallowing.

© 2014 Elsevier Inc. All rights reserved.

at-sen, China.01460 and 81371441 from the100022 from the Guangzhouykpy38 from the Fundamental

ghts reserved.

1. Introduction

Bolus volume is an importantmodulator of the biomechanical eventsthat occur during oropharyngeal swallowing [1]. In the case of variedvolume bolus swallows, volume accommodation guarantees the safetyand efficacy of swallowing.While patients with neurologically impaireddysphagia may face the risk of penetration and aspiration with increasein bolus volume, decrease in bolus volume beyond a certain extent maynot trigger the automatic swallowing reflex [2]. Therefore, alterations inbolus volume can bring about changes in swallowingphysiology inwaysthat can compensate for or exacerbate deficits. Volume modification in

47T. Lin et al. / Physiology & Behavior 128 (2014) 46–51

dysphagia patients has already been employed in routine clinicaltherapy.

To understand the pathology of swallowing, we need to identify thecharacteristics of normal swallowing physiology. Previous studies usedtechniques like ultrasonography [3], videofluoroscopy [2,4–9], electromy-ography [10–12] and traditional manometry [9,13–18] to determine theeffect of bolus volume on pharyngeal swallowing. However, the resultsof these studies were inconsistent, owing to discrepancies in designsand methods, relatively small number of subjects, and different defini-tions for the variables used.Moreover, ultrasonography, videofluoroscopyand electromyography techniques cannot provide adequate quantizationof pharyngeal propulsive force, UES squeezing tone and timing of thecoordination between the pharyngeal contraction and UES relaxation.Previous studies using traditional manometry have contributed to ourknowledge regarding bolus volume on pharyngeal swallowing physiolo-gy [13–18]. However, traditionalmanometric catheters have been provedunsuitable due to only a small number of sensors and rostral movement(2–4 cm) of the UES during the course of swallowing [14]. Besides, unidi-rectional sensors are inappropriate for using in an asymmetric pharynx,since pharyngeal pressure is 2 to 3 times higher in the anterior andposterior directions than in the lateral directions [19,20]. Therefore,traditional manometry fails to offer a comprehensive analysis ofpharyngeal and UES physiological characteristics.

Solid-state high-resolutionmanometry (HRM)provides technologicaladvances over conventional manometry, which has overcome previousequipment shortcomings and allows accurate measurements of therapid response of striated muscle, regardless of the asymmetric pressuredistribution of the pharynx and UES. Using solid-state HRM, Ghosh et al.[21] performed a detailed analysis of deglutitive UES function in normalindividuals during 1 ml, 5 ml, 10 ml, and 20 ml water swallowing andfound that UES relaxation duration and peak pharyngeal contractionincreased with bolus volume. Similarly, Hoffman et al. [22] determinedthe effect of bolus volume on pharyngeal swallowing in 12 healthysubjects using solid-state HRM, and reported an increase in peakvelopharyngeal pressure, velopharyngeal pressure duration, UESopening duration and UES residual pressure as the bolus volumeincreases. However, neither of the aforementioned studies investigatedvolume effect on pharyngeal swallowing by using bolus of differentviscosities, and did not focus on the hypopharynx.

Accurate identification of bolus volume effect is crucial to ourunderstanding of normal and dysfunctional swallowing. This studyexamined how bolus volume can affect hypopharyngeal and upperesophageal sphincter pressure, duration and velocity measurementsduring the process of swallowing in 34 healthy subjects, using thenovel solid-state HRM test.

2. Materials and methods

2.1. Participants

Thirty-four young healthy volunteers (age range = 20–45 years;mean age = 24.3 ± 5.93 years; gender equally represented) wereenrolled in the study. All participants were in good health withoutsymptomsor history of swallowing difficulty, reflux symptoms,medica-tions known to interfere with swallowing, speech disorders, structuraldisorders, cognitive disorders or neurologic and/or muscular diseases.Informed consent was acquired from each participant before datacollection. Ethics approvalwas obtained from the clinical research ethicscommittee of the third affiliated hospital of Sun Yat-sen University.

2.2. High resolution manometry

This study featured a solid-state manometric assembly with 4.2 mmoutside diameter and having 36 circumferential sensors spaced at 1-cmintervals (Sierra Scientific Instruments, Los Angeles, CA). This deviceuses proprietary pressure transduction technology (TactArray) that

allows each of the 36 pressure sensing elements to detect pressure overa length of 2.5 mm in each of 12 circumferentially dispersed sectors.The sector pressures are then averaged to obtain a mean pressure mea-surement, making each of the 36 sensors a circumferential pressuredetector with the extended frequency response characteristic of solid-state manometric systems. Before recording, the transducers werecalibrated at 0 and 300mmHg using externally applied pressure, accord-ing to manufacturer specifications. The response characteristics of eachsensing element were such that they could record pressure transientsin excess of 6000 mm Hg/s and were accurate to within 1 mm Hg ofatmospheric pressure after thermal calibration correction. The dataacquisition frequency was 35 Hz for each sensor. All pressure measure-ments were referenced to atmospheric pressure [23].

2.3. Data collection

After a brief interview, an examinationwas performed to ensure theabsence of gastrointestinal symptoms. The participants then underwenttransnasal placement of the manometric assembly in a natural sittingposition with the head in neutral position. Real-time pressure imagingduring catheter intubation enabled accurate placement. The catheterwas fixed in place by taping it at the nostril. Following a quiet restingadaptation period (up to 10 min) each participant was instructed toswallow3ml, 5ml, and 10ml ofwater, thick liquid, and pastematerials,respectively. All consistencies were prepared 5 min prior to use. Slip tipsyringes were used to measure liquid and paste volumes to ensure thatthe bolus quantities were accurate.

Water at room temperature was combined with Simply & Thicker®(Nestle Nutrition) to prepare the thick liquid and pastes. Both thickliquid and pastes were prepared consistently following this protocol:100ml of water combinedwith 1 tablespoon+ 1 teaspoon of thickener(thick liquid), 100 ml of water combined with 2 tablespoons + 2teaspoon of thickener (paste). The mixtures were stirred and left tostand for 5 min prior to use.

Once the bolus was placed in the mouth, each participant wasinstructed to breath gently through the nose. Each physiologic channelwas monitored to obtain baseline levels. The participant was theninstructed to swallow, and all manometric data were recorded on themanometer during the respective examinations. A total of nine swallows(water, thick liquid, and pastematerial in 3ml, 5ml, and 10ml amounts,respectively) were measured from each participant at each assessmenttime point.

2.4. Data analysis

Pressure and timing data were initially analyzed using ManoViewanalysis software (Sierra Scientific Instruments, Los Angeles, CA).According to the methods of McCulloch [24] and Takasaki [23], the pha-ryngeal region was defined as the area of swallow related pressurechange, with a high pressure zone identified approximately midwaybetween the nasopharynx and the UES, with its epicenter at the highpressure point and extending 2 cm proximal and distal to that point. Inthe present study, the hypopharyngeal region was defined as the areabetween velopharyngeal and the UES. The UES region was defined asthe midpoint of stable high pressure just proximal (rostral) to the base-line low esophageal pressure zone, extending to a point of low esophage-al pressure distally and low baseline pharyngeal pressure proximally[23,24]. During swallowing, this anatomic area is mobile along the cath-eter, moving rostrally as much as 2–4 cm [14].

Values were recorded for maximum pressure, maximum pressurerise rate and duration of pressure above baseline in the regions ofthe hypopharynx, UES residual pressure, UES relaxation duration,maximum preopening UES pressure and maximum postclosure UESpressure. Duration of pressure above baseline within a region wasdefined as the time duration between the onset of pressure escalationand its return to, or below, baseline using the single sensor where

48 T. Lin et al. / Physiology & Behavior 128 (2014) 46–51

maximum pressure was recorded. Maximum pressure rise rate wascalculated by subtracting baseline pressure from maximum pressureand dividing by the time lapse between these points [24].

2.5. Statistical analysis

Repeated measures of one-way analysis of variance were used tocompare bolus volume effects onmeasures of pharyngeal biomechanics.Mauchly's test of sphericity, which tests the null hypothesis that theerror covariance matrix of the orthonormalized transformed dependentvariables is proportional to an identity matrix, was used to inspectrepeated measures effects [16]. In cases where necessary, epsilon-adjusted degrees of freedom were used for the average tests of signifi-cance, and corrected Greenhouse–Geisser P values were adopted.Bonferroni method was used for multiple comparisons and P b 0.05indicated statistical significance. Data was presented as mean ± SD forpressure, velocity and timing events for swallowing ofwater, thick liquid,and paste in Tables 1–3, respectively. All analyses were conducted usingSPSS statistics 19.0 (IBM Corporation, Somers, NY).

3. Results

3.1. UES residual pressure

Significant volume effects were found to be associated with water(F(2,66) = 4.507, P = 0.015) and paste (F(1.44,47.63) = 7.775, P = 0.003)bolus material. Multiple comparisons revealed significant differencesbetween 5 ml and 10 ml amounts of water (P = 0.012), 3 ml and10 ml amounts of paste (P = 0.022), and 5 ml and 10 ml amounts(P= 0.008) of paste, along with an increase in UES residual pressurein relation to an increased bolus volume (Tables 1–3). While thevolume effect during thick liquid swallowing did not reach statisticalsignificance (F(2,66) = 2.886, P = 0.063), there was an increasingtrend in UES residual pressure as the volume increased (Fig. 1).

3.2. UES relaxation duration

Discernible differences were observed between water (F(2,66) =3.530, P = 0.035), thick liquid (F(1.64,54.18) = 7.425, P = 0.003) andpaste (F(1.58,54.07) = 13.155, P b 0.001) deglutition (Tables 1–3).Furthermore, multiple comparisons indicated that differences existedbetween the 3 ml and 10 ml (P = 0.010) and 5 ml and 10 ml (P =0.002) amounts of thick liquid swallows. There were also differencesin UES relaxation between the 3 ml and 5 ml (P = 0.042), 3 ml and10 ml (P b 0.001) as well as 5 ml and 10 ml (P = 0.038) pastevolumes. UES relaxation duration was found to increase with anincrease in bolus volume (Fig. 1). However, during water swallowing,the differences between the three bolus volumes did not reach statisti-cal significance.

Table 1Summary of data during water swallowing.

Variables 3 ml

UES residual pressure (mm Hg) −6.8 ± 3.8UES relaxation duration (s) 0.687 ± 0.127Maximum preopening UES pressure (mm Hg) 124.9 ± 82.7Maximum postclosure UES pressure (mm Hg) 268.7 ± 94.8Maximum hypopharyngeal pressure (mm Hg) 219.8 ± 109.6Maximum hypopharyngeal pressure rise rate (mm Hg/s) 1207.1 ± 1027.8Hypopharyngeal pressure duration (s) 0.442 ± 0.166

Values are means ± SD. UES — upper esophageal sphincter. F — F statistics.⁎ P b 0.05.

3.3. Maximum preopening and postclosure pressure of UES

No significant changes were detected in maximum preopening UESpressure and maximum postclosure UES pressure with relation to thebolus volume for all three materials (Tables 1–3).

3.4. Maximum hypopharyngeal pressure and pressure rise rate

Bolus volume did not appear to have any significant effect onthe maximum hypopharyngeal pressure or pressure rise rate duringwater, thick liquid, and paste swallows (Tables 1–3). Nevertheless, themaximum hypopharyngeal pressure was found to decrease withincrease in bolus volume during thick liquid swallowing (Fig. 1).

3.5. Hypopharyngeal pressure duration

No significant volume effects were observed on measures ofhypopharyngeal pressure duration during the course of water, thickiquid or paste deglutition (Tables 1–3).

4. Discussion

In this study, each participant was asked to finish nine swallowsof water, thick liquid and paste. Using solid-state high-resolutionmanometry (HRM), we determined the effects of bolus volume onpressure, duration and velocity of the hypopharynx and UES duringpharyngeal swallowing. Bolus volume was found to significantlyaffect UES residual pressure and UES relaxation duration, especiallyduring larger-volume swallows. However, maximum preopeningUES pressure, maximum postclosure UES pressure and hypopharynxdid not seem to be affected by bolus volume.

As reported in several other studies, UES residual pressure has adirect relationship with bolus volume, that is, a smaller bolus generallygenerates greater negative pressure [13,17,21,22]. The negative UESresidual pressure is considered to act as a “suction pump”, pulls thebolus into the esophagus [25], and is therefore believed to be the mostimportant parameter for the assessment of UES function. In the case oflarge-volume bolus, the “suction pump” effect is less pronouncedsince higher gravity and longer UES opening duration are sufficient forbolus to pass through the UES into the esophagus. However, in mostof the aforementioned studies, the UES pressures were all above zero.This was primarily because the former studies were conducted withthe patients in a supine position, which resulted in the elevation ofthe diaphragm leading to an increase in intrapleural pressure. In thisposition there is higher downstream resistance, leading to increases inthe UES residual pressure. In addition, the use of two strain-gaugemanometric probeswith only a few transducers spaced at 3 cm intervalsmay have resulted in failure to capture the accurate pressures inducedby UES elevation [26,27].

In the present study, we demonstrated the effect of bolus volume onUES relaxation duration which was in line with prior studies where

5 ml 10 ml F P

−7.5 ± 4.0 −5.8 ± 4.6 4.507 0.015⁎

0.690 ± 0.121 0.722 ± 0.133 3.530 0.035⁎

136.7 ± 86.8 133.9 ± 68.0 1.157 0.321260.0 ± 90.0 281.3 ± 86.2 1.483 0.234205.5 ± 85.5 190.7 ± 89.0 2.590 0.093

1087.6 ± 707.9 1009.1 ± 528.5 0.896 0.3660.427 ± 0.146 0.415 ± 0.135 1.200 0.308

Table 2Summary of data during Thick Liquid Swallowing.

Variables 3 ml 5 ml 10 ml F P

UES residual pressure (mm Hg) −7.3 ± 4.7 −7.0 ± 4.9 −5.9 ± 4.7 2.886 0.063UES relaxation duration (s) 0.659 ± 0.128 0.669 ± 0.130 0.702 ± 0.129 7.425 0.003⁎

Maximum preopening UES pressure (mm Hg) 113.8 ± 68.4 111.6 ± 69.7 105.2 ± 58.5 0.752 0.475Maximum postclosure UES pressure (mm Hg) 232.7 ± 73.8 242.2 ± 90.9 251.3 ± 75.0 2.085 0.132Maximum hypopharyngeal pressure (mm Hg) 202.5 ± 95.7 201.8 ± 102.7 173.5 ± 68.9 3.514 0.061Maximum hypopharyngeal pressure rise rate (mm Hg/s) 1077.7 ± 624.2 1132.0 ± 876.4 921.5 ± 546.5 1.639 0.206Hypopharyngeal pressure duration (s) 0.406 ± 0.157 0.413 ± 0.150 0.397 ± 0.127 0.723 0.466

Values are means ± SD. UES — upper esophageal sphincter. F — F statistics.⁎ P b 0.05.

49T. Lin et al. / Physiology & Behavior 128 (2014) 46–51

increase in bolus volume resulted in prolonged UES relaxation[4,16,21,22,28]. Increase in bolus volume caused the anterior hyoidmovement to occur earlier during the swallow sequence in order toaccommodate the early entry of large boluses into the pharynx [29].However, values of UES relation duration reported in the literature arenot consistent due to varying definitions of UES relaxation. Usingmanometry, UES relaxation duration has been measured as 0.6 to1.0 s, while the average relaxation time measured by cricopharyngealelectromyography is 0.3 s [30]. However, another study by Gumbleyet al. [17] reported novolume effect onUES relaxation duration between5 ml, 10 ml, and 20 ml water bolus swallows. Interestingly, conflictingresults have been obtained from several other studies using electromy-ography (EMG); for example, Ertekin et al. [11] reported that thecricopharyngeal EMG pause increased significantly with increasingbolus volume, while Perlman et al. [10] discovered that the totalduration of cricopharyngeal EMG activity did not change with bolusvolume. Therefore, the effect of bolus volumeonUES relaxation durationstill needs to be elucidated, with the prerequisite that the definition ofUES relaxation is standardized.

Few studies have focused on the influence of bolus volume onmaximum preopening UES pressure and maximum postclosure UESpressure. We found no significant volume effects on these two parame-ters during all three kinds of bolus swallowing, which is in line withthe findings from a recent study by Hoffman et al. [22] who investigatedthe effect of varied volume (saliva, 5 ml, 10 ml and 20 ml) onmaximumUES preopening and postclosure pressure.We deduced that the functionof the maximum preopening UES pressure was to avoid early entry ofbolus into the esophagus, while themaximum postclosure UES pressurecontributed to preventing bolus reflux. Therefore,maximumpreopeningand postclosure UES pressure are primarily involved in controlling bolusmovement, and this function does not seem to be affected by bolusvolume. However, further research is needed to confirm this hypothesis.

Pharyngeal contraction pressure has been described as a “propulsionpump” [25], pushing a bolus through the UES into the esophagus. Inaccordance with previous research, we found no linear relationshipsbetween bolus volumes and the amplitude and duration of pharyngealcontraction pressure [6,14,17,31,32]. Nevertheless, Butler et al. [16]used simultaneous manometry and endoscopy, and found maximum

Table 3Summary data during paste swallowing.

Variables 3 ml

UES residual pressure (mm Hg) −7.6 ± 4.6UES relaxation duration (s) 0.644 ± 0.139Maximum preopening UES pressure (mm Hg) 111.3 ± 80.8Maximum postclosure UES pressure (mm Hg) 253.7 ± 106.6Maximum hypopharyngeal pressure (mm Hg) 187.4 ± 72.0Maximum hypopharyngeal pressure rise rate (mm Hg/s) 954.1 ± 587.9Hypopharyngeal pressure duration (s) 0.410 ± 0.142

Values are means ± SD. UES — upper esophageal sphincter. F — F statistics.⁎ P b 0.05.

pharyngeal pressure to increase with the increase in bolus volume.However, this result may be not precise, since the manometric catheterused in their study had only three solid-state, unidirectional and poste-rior oriented sensors, which is unsuitable for the pharyngoesophagealsegment, due to the radially asymmetric contraction pressure as wellas the rapid rate of contraction. Moreover, it was possible that thethree sensors were ineffective when the UES moved cephally duringswallowing. Although no statistically significant volume effect wasdetected in our research, we found that as bolus volume increased,maximum hypopharyngeal pressure presented with a trend of decline,especially in water and thick liquid swallows, which was in tandemwith the UES relaxation duration discussed above. We have alwaysheld the opinion that pharyngeal contraction was in cooperation withUES opening [33,34]. It is possible that prolonged UES relaxationduration is sufficient for increased bolus to pass the UES, so there is noneed to increase the contraction force of pharyngealmuscles.Moreover,while accommodating larger bolus, the anterosuperior excursion of thehyoid increases to create a larger cavity [3,35,36] and the period oflaryngeal elevation is prolonged [14], which leads to lower pressuresin the hypopharynx. However, during the process of paste swallowing,the decrease in maximum hypopharyngeal pressure is disturbed bythe increase in resistance, which is likely the reason for no evidentdecline of the maximum hypopharyngeal pressure with rise in bolusvolume.

To our knowledge, the effect of bolus volume on pharyngealpressure rise rate has not been reported. We found no discernabledifference in maximum hypopharyngeal pressure rise rate during thedeglutition of the three materials in the present study. This is in accor-dance with the previous studies wherein the velocity of pharyngealcontractions was stable regardless of bolus volume increase [14,37].On the other hand, Hoffman et al. [22] reported that tongue basepressure rise rate decreased discernibly as bolus volume was increased,although this study was limited to the use of water bolus only. Ashypopharyngeal constrictors are skeletal muscles, with rapid contrac-tions and pressure rise rates up to 600 mm Hg/s [38], maximumpressure rise rate is considered to be an appropriate index to mirrormuscle contraction function. In the present study, volume had no effectonmaximumhypopharyngeal pressure rise rate, which is primarily due

5 ml 10 ml F P

−7.4 ± 4.9 −5.8 ± 4.6 7.775 0.003⁎

0.671 ± 0.165 0.715 ± 0.128 13.155 b0.001⁎

100.8 ± 69.5 101.3 ± 77.5 0.769 0.424244.8 ± 67.3 254.8 ± 82.5 0.463 0.632187.0 ± 67.7 180.9 ± 72.3 0.427 0.654888.7 ± 381.0 792.5 ± 342.4 2.352 0.1180.399 ± 0.103 0.426 ± 0.116 0.971 0.368

3ml 5ml

10ml

Fig. 1. Spatiotemporal plots from one subject while swallowing 3ml, 5 ml, and 10 ml amounts of thick liquid. As bolus volume increases, UES relaxation duration (white two-way arrow)and UES residual pressure (dashed white arrow) increase, while maximum hypopharyngeal pressure (solid white arrow) shows a trend of decline.

50 T. Lin et al. / Physiology & Behavior 128 (2014) 46–51

to the rise in bolus volume, leading to reduction in both maximumhypopharyngeal pressure and the maximum hypopharyngeal pressurerise time.

In the present study, no regular changes in hypopharyngeal pressuredurationwere detectedwith the three kinds of bolus swallows. This is inaccordancewith results from the previous studies [13,15–17,31,39]. Thelikely interpretation is that contraction strength of hypopharyngealconstrictors contributes more to cleaning residual bolus than driving itforward, and this function is independent of bolus volume. Furthermore,bolus volume increase is accompanied by a faster flow rate, which isinduced by greater bolus gravity, resulting in the absence of volumeeffect on hypopharyngeal pressure duration. It has been reported thatbolus viscosity, gender, and age play important roles in hypopharyngealpressure duration [15,31,39]. Further research on hypopharyngealpressure duration should take all these factors into consideration, inorder to obtain a better understanding of physiological swallowing.

High-resolution manometry (HRM) has fast replaced traditionalmanometry to become the gold standard for studying pharyngeal andesophageal motility. With optimal spatial and temporal resolution, 36circumferential sensor arrays spaced 1 cm apart, and the ability todetect rapid pressure changes, HRM has overcome the conventionalmanometry shortcomings of limited sensors, unidirectional sensoring,incorrect anatomical location and slow response to pressure variations[24,26,40]. Additional and perhaps subtle findings previously undetect-able with traditional manometry may be captured by HRM. Hence,HRM reveals more accurate and comprehensive swallowing functions,especially pharyngeal swallowing.

High UES residual pressure, short UES relaxation duration, weakpharyngeal contraction and UES/pharyngeal incoordination are commonclinical symptoms of dysphagia. Solid-state high-resolution manometryis currently the gold standard for the detection of swallowing disorders.A clear understanding of bolus volume effect on hypopharynx and UES

will provide us with theoretical guidance for rehabilitation in patientswith dysphagia, involving food adjustment. While several significantdifferenceswere observed between 3ml, 5ml and 10ml volumes duringwater, thick liquid and paste swallowing, there were three limitations tothis study. Firstly, the sample size was relatively small. Secondly, most ofthe participants involved in this study were young adults. Furtherresearch should be conducted in different age groups in order to get asystematic and comprehensive conclusion. Thirdly, all of the participantsin this investigation were normal individuals. Manometric measure-ments from individuals with abnormal swallowing may produce resultsdifferent from those observed in the present study.

5. Conclusion

Solid-state high-resolution manometry of the pharynx and the UESprovides important information regarding the effect of swallowing onpharyngeal contraction and relaxation of the UES. Our findings indicatethat bolus volume has a significant effect on UES residual pressureand UES relaxation duration, andmay affectmaximumhypopharyngealpressure, and this volume effect is likely to be influenced by bolusviscosity. Further research involving the effect of bolus volume willextend the current knowledge of biomechanical events in the hypo-pharynx and UES and provide us with theoretical guidance duringclinical practice. Broader studies including larger cohorts of both normalsubjects and dysphagia patients of different ages, heights and gendersmight provide us with more insight into the underlying mechanismsof swallowing physiology and pathology.

References

[1] Kahrilas PJ, Logemann JA. Volume accommodation during swallowing. Dysphagia1993;8:259–65.

51T. Lin et al. / Physiology & Behavior 128 (2014) 46–51

[2] Bisch EM, Logemann JA, Rademaker AW, Kahrilas PJ, Lazarus CL. Pharyngeal effects ofbolus volume, viscosity, and temperature in patients with dysphagia resulting fromneurologic impairment and in normal subjects. J Speech Hear Res 1994;37:1041–59.

[3] Chi-Fishman G, Sonies BC. Effects of systematic bolus viscosity and volume changeson hyoid movement kinematics. Dysphagia 2002;17:278–87.

[4] Williams RB, Pal A, Brasseur JG, Cook IJ. Space-time pressure structure ofpharyngo-esophageal segment during swallowing. Am J Physiol GastrointestLiver Physiol 2001;281:G1290–300.

[5] Jacob P, Kahrilas PJ, Logemann JA, Shah V, Ha T. Upper esophageal sphincter openingand modulation during swallowing. Gastroenterology 1989;97:1469–78.

[6] Kahrilas PJ, Logemann JA, Lin S, Ergun GA. Pharyngeal clearance duringswallowing: a combined manometric and videofluoroscopic study.Gastroenterology 1992;103:128–36.

[7] Chi-Fishman G, Sonies BC. Motor strategy in rapid sequential swallowing: newinsights. J Speech Lang Hear Res 2000;43:1481–92.

[8] Rademaker AW, Pauloski BR, Colangelo LA, Logemann JA. Age and volumeeffects on liquid swallowing function in normal women. J Speech Lang HearRes 1998;41:275–84.

[9] Kahrilas PJ, Lin S, Logemann JA, Ergun GA, Facchini F. Deglutitive tongue action:volume accommodation and bolus propulsion. Gastroenterology 1993;104:152–62.

[10] Perlman AL, Palmer PM, McCulloch TM, Vandaele DJ. Electromyographic activityfrom human laryngeal, pharyngeal, and submental muscles during swallowing. JAppl Physiol 1999;86:1663–9.

[11] Ertekin C, Aydogdu I, Yuceyar N, Pehlivan M, Ertas M, Uludag B, et al. Effects ofbolus volume on oropharyngeal swallowing: an electrophysiologic study inman. Am J Gastroenterol 1997;92:2049–53.

[12] Dantas RO, Dodds WJ. Effect of bolus volume and consistency on swallow-inducedsubmental and infrahyoid electromyographic activity. Braz J Med Biol Res1990;23:37–44.

[13] Dantas RO, Kern MK, Massey BT, Dodds WJ, Kahrilas PJ, Brasseur JG, et al. Effect ofswallowed bolus variables on oral and pharyngeal phases of swallowing. Am JPhysiol 1990;258:G675–81.

[14] Kahrilas PJ, Dodds WJ, Dent J, Logemann JA, Shaker R. Upper esophageal sphincterfunction during deglutition. Gastroenterology 1988;95:52–62.

[15] Perlman AL, Schultz JG, VanDaele DJ. Effects of age, gender, bolus volume, andbolus viscosity on oropharyngeal pressure during swallowing. J Appl Physiol1993;75:33–7.

[16] Butler SG, Stuart A, Castell D, Russell GB, Koch K, Kemp S. Effects of age, gender,bolus condition, viscosity, and volume on pharyngeal and upper esophagealsphincter pressure and temporal measurements during swallowing. J Speech LangHear Res 2009;52:240–53.

[17] Gumbley F, HuckabeeML, Doeltgen SH,Witte U, Moran C. Effects of bolus volume onpharyngeal contact pressure during normal swallowing. Dysphagia 2008;23:280–5.

[18] Pouderoux P, Kahrilas PJ. Deglutitive tongue force modulation by volition, volume,and viscosity in humans. Gastroenterology 1995;108:1418–26.

[19] Dodds WJ. Physiology of swallowing. Dysphagia 1989;3:171–8.[20] Sears Jr VW, Castell JA, Castell DO. Radial and longitudinal asymmetry of human

pharyngeal pressures during swallowing. Gastroenterology 1991;101:1559–63.[21] 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.

[22] Hoffman MR, Ciucci MR, Mielens JD, Jiang JJ, McCulloch TM. Pharyngeal swallowadaptations to bolus volumemeasuredwith high-resolutionmanometry. Laryngoscope2010;120:2367–73.

[23] Takasaki K, Umeki H, Enatsu K, Tanaka F, Sakihama N, Kumagami H, et al.Investigation of pharyngeal swallowing function using high-resolution manometry.Laryngoscope 2008;118:1729–32.

[24] McCulloch TM, Hoffman MR, Ciucci MR. High-resolution manometry of pharyngealswallow pressure events associated with head turn and chin tuck. Ann Otol RhinolLaryngol 2010;119:369–76.

[25] Cerenko D, McConnel FM, Jackson RT. Quantitative assessment of pharyngeal bolusdriving forces. Otolaryngol Head Neck Surg 1989;100:57–63.

[26] Fox MR, Bredenoord AJ. Oesophageal high-resolution manometry: moving fromresearch into clinical practice. Gut 2008;57:405–23.

[27] Takasaki K, Umeki H, Kumagami H, Takahashi H. Influence of head rotation on upperesophageal sphincter pressure evaluated by high-resolution manometry system.Otolaryngol Head Neck Surg 2010;142:214–7.

[28] Babaei A, Dua K, Naini SR, Lee J, Katib O, Yan K, et al. Response of the upperesophageal sphincter to esophageal distension is affected by posture, velocity,volume, and composition of the infusate. Gastroenterology 2012;142:734–43[e7].

[29] Cook IJ, DoddsWJ,Dantas RO,Massey B, KernMK, Lang IM, et al. Openingmechanismsof the human upper esophageal sphincter. Am J Physiol 1989;257:G748–59.

[30] Bhatia SJ, Shah C. How to perform and interpret upper esophageal sphinctermanometry. Neurogastroenterol Motil 2013;19:99–103.

[31] Shaker R, Ren J, Podvrsan B, Dodds WJ, Hogan WJ, Kern M, et al. Effect of aging andbolus variables on pharyngeal and upper esophageal sphincter motor function. Am JPhysiol 1993;264:G427–32.

[32] Castell JA, Dalton CB, Castell DO. Effects of body position and bolus consistency onthe manometric parameters and coordination of the upper esophageal sphincterand pharynx. Dysphagia 1990;5:179–86.

[33] Kahrilas PJ, Lin S, Chen J, Logemann JA. Oropharyngeal accommodation to swallowvolume. Gastroenterology 1996;111:297–306.

[34] Mendell DA, Logemann JA. Temporal sequence of swallow events during theoropharyngeal swallow. J Speech Lang Hear Res 2007;50:1256–71.

[35] Dodds WJ, Man KM, Cook IJ, Kahrilas PJ, Stewart ET, Kern MK. Influence of bolusvolume on swallow-induced hyoid movement in normal subjects. AJR Am JRoentgenol 1988;150:1307–9.

[36] Ergun GA, Kahrilas PJ, Lin S, Logemann JA, Harig JM. Shape, volume, and content ofthe deglutitive pharyngeal chamber imaged by ultrafast computerized tomography.Gastroenterology 1993;105:1396–403.

[37] Castell JA, Dalton CB, Castell DO. Pharyngeal and upper esophageal sphinctermanometry in humans. Am J Physiol 1990;258:G173–8.

[38] Cook IJ, Kahrilas PJ. AGA technical review on management of oropharyngealdysphagia. Gastroenterology 1999;116:455–78.

[39] Yokoyama M, Mitomi N, Tetsuka K, Tayama N, Niimi S. Role of laryngeal movementand effect of aging on swallowing pressure in the pharynx and upper esophagealsphincter. Laryngoscope 2000;110:434–9.

[40] Mielens JD, Hoffman MR, Ciucci MR, Jiang JJ, McCulloch TM. Automated analysis ofpharyngeal pressure data obtained with high-resolution manometry. Dysphagia2011;26:3–12.