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Oropharyngeal swallowing hydrodynamics of thin and mildly thick liquids in an anatomically accurate throat-epiglottis model – Scientific Reports

Liquid viscosity and liquid-wall contact angle

Methyl cellulose solution viscosities

Figure 3 shows the measured viscosity of Methyl Cellulose (MC) solutions at varying concentrations (1–2% w/v). The mean viscosity increased quickly with the MC concentration, from 245 ± 8 at 1%, to 1922 ± 197 mPaˑs at 2%. To consider the shear-thinning effect, the MC solutions were measured at different rotation rates with corresponding spindles (Fig. 3b–e). For each solution, the viscosity decreases with increasing shear rate. However, the slope of their profiles differs significantly, which is approximately − 0.41, − 0.48, − 1.76, and − 10.1 mPaˑs/rpm for 1%, 1.1%, 1.2%, and 2% w/v MC solutions, respectively (Fig. 3b–e). According to the Pureed texture categorization55,56,57,58, the 1% w/v MC solution are still thin liquid but closely approaching ‘nectar” consistency liquid (i.e., 300–1500 mPaˑs). The 2% w/v MC solution belongs to “honey” consistency thickened liquid that has a range of 1500–3000 mPaˑs.

The surface tension was measured to be 72.11 ± 0.37 mN/m for water and 79.81 ± 0.86 m N/m for 1% w/v MC solution. Different liquid behaviors are expected, particularly in confined spaces like the vallecula and esophagus opening, where surface tension influences liquid bank formation or breakup. A higher surface tension may cause liquid bridging over the esophagus opening and prevent the liquid from entering the esophagus, while a lower surface tension may facilitate a smoother entrance.

Contact angle of MC solutions on model materials

Figure 4 shows the contact angles on the three materials for water and MC solutions with three concentrations (1%, 1.1%, and 1.2% w/v). For all liquids considered, the silicone rubber exhibited the highest contact angle, followed by the elastic 50A SLA, while the rigid transparent SLA demonstrated the smallest angle, indicating a superior wettability on the rigid transparent SLA than on the other two materials. Water had a larger contact angle than the MC solutions on the silicone rubber and elastic 50A SLA, but a lower contact angle on the rigid transparent SLA. In particular, the water contact angle decreased drastically from silicone rubber (115°) to elastic 50A SLA (90°), and then to rigid transparent SLA (35°). A similar trend was also found for MC solutions but with a smaller decrease in magnitude. Moreover, the MC solution contact angle decreased slightly with increasing concentration for the three materials considered. The variations in contact angle indicate different fluid behaviors on various test materials, highlighting the need to consider potential differences in fluid behaviors between in vivo tissues and in vitro materials.

Figure 4
figure 4

Contact angles for various formulations on: (a) silicone rubber, (b) elastic 50A SLA, and (c) rigid transparent SLA.

Deglutition tests using 50A SLA full-throat model

Liquid motions and aspirations were systemically studied under four dispensing conditions: fast posterior, slow posterior, fast anterior, and slow anterior. Each condition was repeated at least three times. Negligible aspirations were observed under the slow posterior dispensing condition. With the aim of identifying factors leading to aspiration, only results of the other three conditions are presented in the following sections.

Fast dispense of water to the posterior oropharynx

Figure 5, as well as the supplemental video S1, shows the hydrodynamics for fast dispensing of water (i.e., 5 mL within 1 s) to the posterior oropharynx. The fast-dispensed water was deflected upon impaction and bifurcated into two streams. The curved oropharyngeal wall was directly above the pharyngeal space, which facilitated the deflected water to reach the tongue base. This small portion of water streamed downward within the upper pyriform fossae (i.e., the groove between the lateral pharynx and epiglottis), entering the lower pyriform fossa (or sinus); an even smaller portion entered the laryngeal vestibule via the recesses above and below the cuneiform tubercle. The latter caused a stream of aspiration, as shown in the middle lateral wall of the trachea (red arrow, fifth panel, Fig. 5). Due to fast dispensing, the water line in the pyriform fossa rose beyond the interarytenoid notch, leading to overflow through the notch, forming a stream along the dorsal trachea (pink arrow, fifth panel, Fig. 5).

Figure 5
figure 5

Temporospatial hydrodynamics of water being fast dispensed to the posterior oropharynx. Also shown in the supplemental video recording S1.

On the other hand, the majority of water flowed down along the dorsal pharynx wall and accumulated in the pyriform fossa before entering the esophagus, as illustrated in the first five panels. This process was quick, lasting 1.27 s till the fifth panel. The 45°-down-tilt epiglottis acted as an umbrella, guiding the water into the esophagus through the clearance between the epiglottis tip and the dorsal pharynx (yellow arrow, fourth panel, Fig. 5). Water was found in the connecting interface between the oropharynx and pharynx (white hollow arrow, second panel, Fig. 5), indicating the high sensitivity of thin liquids like water to geometrical details (including both the anatomical complexities and experimental imperfections).

Fast dispense of water to the anterior oropharynx

Figure 6, as well as the supplemental video S2, shows the hydrodynamics of fast water dispensing (i.e., 5 mL over 1 s) to the anterior oropharynx in the full-throat model, with the three panels exhibiting the start, middle, and end of water dispensing (indicated by the remaining volume in the syringe). In this case, the effects of gravity and inertia were more pronounced than in the previous case. The water flowed quickly along the tongue base and ventral pharynx. Upon impinging on the upper epiglottis, the water spread over it, with some flowing over the epiglottis edge (or aryepiglottic fold), as demonstrated by the streams on the ventral, lateral, and dorsal walls of the pharynx (yellow arrows, Fig. 6). In particular, the liquid stream along the dorsal wall resulted from the water flowing down the 45°-down-tilt epiglottis and through the clearance between the epiglottis tip and dorsal pharynx. Such a liquid stream was absent when the dispensing speed was slow, which will be discussed in the following section (Fig. 7a, first vs. second panels).

Figure 6
figure 6

Temporospatial hydrodynamics of water being fast dispensed to the anterior oropharynx. Also shown in the supplemental video recording S1.

Figure 7
figure 7

Comparison of liquid hydrodynamics and aspiration under varying dispensing conditions (i.e., fast, posterior; fast, anterior; slow, anterior) for: (a) water and (b) 1% w/v MC solution. Fast, anterior: fast dispensing to the anterior oropharynx. The hydrodynamics of water with slow-dispensing and the MC solution with fast-dispensing can also be viewed in the supplemental video recording S3 and S4, respectively.

Three aspiration liquid streams were observed in the trachea, with two in the middle and one at the back (red arrows, Fig. 6). A significant amount of aspiration was collected, close to that of deglutition (rightmost panel, Fig. 6). It is noted that the esophageal opening can be larger than that hereof, as the larynx will move upward and forward, enlarging the esophageal opening and increasing the deglutition rate, thus slowing down the liquid buildup in the pyriform sinus and lowering the chance of overflow into the inter-arytenoid notch.

Slow dispense of water to the anterior oropharynx

Significant aspirations were observed when dispensing water slowly (i.e., 5 mL within 3 s) to the anterior oropharynx (i.e., slow anterior, as shown in the supplemental video S3). Figure 7a compares the aspired fluid, as well as the hydrodynamics around 1.27 s since the start of dispensing, between the slow-anterior condition (middle panel) and the conditions of fast-anterior (first panel) and fast-posterior (third panel). Due to slow dispensing, surface tension played a more significant role than gravity or kinetic energy. The low speed allowed the liquid stream to cling to the arch of the tongue base, which then diverted to two sides (yellow arrow) when reaching the vallecula and subsequently moved down through the upper pyriform fossa. A substantial fraction of water flowed along the aryepiglottic folds, with some of it entering the laryngeal vestibule via the recesses above and below the cuneiform tubercle. This was evidenced by the larger amount of water collected under the trachea than in the esophagus (second panel, Fig. 7a). Aspiration occurred at the middle lateral trachea wall. The water level in the pyriform sinus remained low, and no overflow via the interarytenoid notch was observed.

Deglutition tests using 50A SLA full-throat model and 1% w/v MC solution

Fast dispense of 1% w/v MC solution to the posterior oropharynx

The first panel in Fig. 7b and the supplemental video S4 show the hydrodynamics of 1% w/v MC solution after fast dispensing to the posterior oropharynx. In contrast to water, no aspiration was observed with the MC solution, either in the trachea or the collecting tray (Fig. 7b vs. a, first panels); this observation was consistent with a much-reduced aspiration risk with a thicker liquid36,37. The flow pattern of the MC solution was more continuous and coherent than that of water, as displayed along the dorsal pharyngeal wall and inside the esophagus (Fig. 7b vs. a, first panels). No MC solution was deflected from the posterior oropharynx to the tongue base during dispensing. Thus, there is no lateral penetration into the laryngeal vestibule via the recesses above or below the cuneiform tubercle. The MC solution level appeared to be higher than the interarytenoid notch; however, notch overflow aspiration was not observed, presumably due to the liquid bridging effects caused by its much higher viscosity and slightly higher surface tension than water.

Fast dispense of 1% w/v MC solution to the anterior oropharynx

No aspiration was observed with a fast dispensing of 1% w/v MC solution to the anterior oropharynx (second panel, Fig. 7b and supplemental video S4). The MC solution followed a clear trajectory, which first moved along the arch of the tongue base, then the upper surface of the slanted epiglottis, followed by a smooth passage through the clearance between the epiglottis tip and dorsal pharynx before entering the esophagus. The fluid stream appeared to be stable throughout the dispensing phase. In comparison to water with significant leaking over the edges of the epiglottis, no edge leaking was noted for the 1% w/v MC solution.

The draining rate into the esophagus (i.e., deglutition rate) was fast, and the liquid level in the pyriform sinus did not rise over the interarytenoid notch. This might result from the smooth flow stream into the esophagus without forming a film blocking the esophagus opening. One counter-example of this hypothesis was the observation of occasional bulging in the water stream, which was completely absent in the MC fluid stream. Such bulging was caused by the sporadic formation of a water film covering the esophagus opening, which temporarily blocked the flow into it, followed by a sudden film rupture and a surge in deglutition flow rate.

Slow dispense of 1% w/v MC solution to the posterior oropharynx

Slow dispensing of MC solution to the anterior oropharynx is shown in the third panel of Fig. 7b. Again, no or negligible aspiration was observed in all three repetitions. The slow dispensing speed allowed more MC solutions to flow along the 45°-down-flapped epiglottis, rather than splitting upon hitting the vallecula and diverting laterally to the upper pyriform fossae. As a result, more fluid moved through the clearance between the epiglottis tip and dorsal pharynx and directly entered the esophagus, minimizing the aspiration risk via notch overflows. Due to a smooth flow into the esophagus, the MC solution level in the lower pyriform fossae was persistently low.

Visualization of overflows and residuals from other views

To verify the phenotypic aspiration mechanisms proposed in this study, water kinematics around the point of interest were recorded from varying angles, including views from the rear, front, and inside (endoscope). Mechanisms to verify consisted of (1) overflow through interarytenoid notch leading to an aspiration stream along the dorsal trachea, (2) overflow through the cuneiform tubercle recesses leading to an aspiration stream on the lateral trachea, and (3) off-edge capillary flow under the epiglottis leading to an aspiration stream along the ventral trachea. An equivalent verification to the last one was whether there was residual accumulation along the conjunction between the down-folded epiglottis and the laryngeal vestibule edge, which was predisposed to drip into the laryngeal vestibule driven by gravity.

Rear view

Figure 8a,b present the rear view of the hydrodynamics under varying intake conditions for 1% w/v MC solution and water, respectively. For a moderately thick fluid like 1% w/v MC solution, symmetric flow patterns were observed throughout the process, as illustrated by equal liquid levels in the two pyriform sinuses in the first two panels in Fig. 8a. Regular flow patterns were also found for the 1% w/v MC solution under slow dispensing to the anterior oropharynx (third panel) or fast dispensing to the posterior oropharynx (fourth panel, Fig. 8a). One difference between these two cases was the liquid level in the pyriform sinuses, which did not build up under the slow dispensing condition due to esophagus drainage. When dispensed from the posterior oropharynx, the MC solution adhered to the dorsal pharynx and directly entered the esophagus, with a lower likelihood of overflow over the interarytenoid notch and nearly no likelihood for overflow over the cuneiform recesses nor off-edge capillary flows. When dispensed to the side oropharynx, the MC solution mainly flowed through the groove between the lateral pharynx and epiglottis, with a small fraction flowing over the upside epiglottis. The slanted liquid level in the pyriform sinus in the rightmost panel in Fig. 8a indicated a lower esophagus drainage rate than the dispensing rate.

Figure 8
figure 8

Rear view of the hydrodynamics in the full-throat model with a 45o down-tilt epiglottis: (a) 1% w/v MC solution, and (b) water. The white arrows denote the occasional formation of a liquid bridge over the esophagus opening. The water motions can also be viewed in the supplemental video recording S5.

In contrast to the coherent flow patterns for the MC solution, water exhibited more irregular patterns and more complex dynamics. Fast dispensing of water to the anterior oropharynx led to a highly transient process, including stream ramifications, coalescence, and splashing, as shown in Fig. 8b and the supplemental video S5. There were three rivulets at the epiglottis tip in the second panel in Fig. 8b, indicating the significance of the epiglottis edge on the water film dynamics. Note that the off-edge flows could lead to aspirations. The hydrodynamics along the epiglottis edge was crucial in determining whether off-edge aspiration occurred or not and in estimating the amount of aspiration under different conditions (e.g., dispensing rate). Water flowed along the rounded edges of the epiglottis more often than the MC solution for any corresponding conditions (Fig. 8b vs. a). Besides, all water flows were observed to be asymmetric (Fig. 8b), as opposed to the symmetry of MC flows (Fig. 8a), indicating unstable hydrodynamics and higher chances for cuneiform recess overflows.

Front view of slow dispensing of water to the anterior oropharynx

Considering that the lateral and rear views cannot clearly visualize the dynamic fluid interactions with the front throat, we further examined the hydrodynamics with a front view of the worst scenario, i.e., slow dispensing of water to the anterior oropharynx (Fig. 9). Five test runs were undertaken with identical dispensing conditions, and aspirating streams in the trachea were observed in all five cases, confirming the susceptibility of this intake scenario. However, different aspiration symptoms were recorded, with a stream along the lateral trachea in two cases (Fig. 9a) vs. along the ventral trachea in four cases, as illustrated by the dashed lines in Fig. 9. Among the five cases with an identical anatomy and intake condition, similarities existed among aspiring liquid streams, i.e., starting from the right cuneiform recess, traveling to the left glottal aperture due to inertia, and bifurcating either to the lateral or ventral trachea (first and second panels, Fig. 9). Further reviewing the video recordings (supplemental video S6) near the glottis also revealed subtle differences among the sources for the aspirating streams along the ventral trachea: the stream starting from the right cuneiform recess traveled directly to the glottis tip and down to the ventral trachea without detouring to the left as in the second panel, likely due to a slower speed of the fluid bolus.

Figure 9
figure 9

Front view of water hydrodynamics of five test cases (1–5) under slow dispensing to the anterior oropharynx with the aspirating streams observed in: (a) lateral trachea (cases 1 and 4), (b) ventral trachea (cases 2, 3, 5), and (c) ventral trachea with a different drop trajectory (cases 1, 3). The hydrodynamics in case 3 can be viewed in the supplemental video recording S6.

Endoscope view of slow dispensing of water to the anterior oropharynx

Endoscope video recording further verified the overflow of water through the recesses above and below the cuneiform tubercle under the anterior slow dispensing condition, as shown by the brown arrow in the middle panel of Fig. 10a. A static image taken at 4 s after dispensing also exhibited residual drops along the overflow path (three brown arrows in the right panel of Fig. 10a). To help understand the endoscope image, a throat cast was displayed in the same direction as the image, with the endoscope camera in position with a side-view mirror to focus on the laryngeal vestibule (left panel, Fig. 10a). Recess overflows below and above the tubercle were illustrated using two red solid arrows, respectively. A water stream falling off the epiglottis tip was also captured (white arrow in the middle panel of Fig. 10a).

Figure 10
figure 10

Endoscope imaging for the case with slow dispensing of water to the anterior oropharynx to capture (a) overflow through the recesses above and below the cuneiform tubercle and (b) residuals under the epiglottis along the flapping line.

Endoscope imaging also captured water residuals under the epiglottis along the flapping line, as shown in Fig. 10b. These residuals indicated that (1) flow splitting occurred after hitting the vallecula, (2) water moved down the convex epiglottis and flowed over the epiglottis edge, and (3) capillary flow formed underneath the epiglottis along the flapping line due to the acute angle of this space, as well as liquid-wall adhesion and liquid–air surface tension.

Silicone-molded half-throat model

Figure 11 shows the hydrodynamics of dispensed liquids to the anterior oropharynx of the silicone-molded half-throat model. A clearer view of the fluid interactions with the epiglottis was obtained, especially around the vallecula, which was visually obscured when using the full-throat model. When fast dispensed to the anterior oropharynx, the 1% w/v MC solution followed a smooth trajectory along the curvature of the tongue base, diverted into the lateral groove upon reaching the vallecula, and accumulated in the pyriform fossa. Esophagus drainage started when 70% of the MC solution was dispensed (yellow arrow, first panel, Fig. 11a). No splashing was observed throughout the process, and the liquid motion was regular. A careful examination also revealed that the four drops near the pharynx and upper trachea resulted from the clearance between the half model and plexiglass and, thus were not indicative of aspiration or penetration. It should also be noted that slight disparities inevitably existed between the half-throat and full-throat experimental setups; one such difference was that the epiglottis in the half model pressing against the dorsal pharynx while a small clearance existed in the full-throat model.

Figure 11
figure 11

Liquid dynamics in the silicone-molded half-throat model with a 45° down-tilt epiglottis for 1% w/v MC solution and water: (a) fast dispensing to the anterior oropharynx, and (b) slow dispensing to the anterior oropharynx.

In comparison to the MC solution, drastically different hydrodynamics were observed when fast-dispensing water to the anterior oropharynx. The water moved much faster from the oropharynx to the esophagus opening, leaving a much thinner coating on the tongue base and vallecula and leading to an earlier onset of esophagus draining (around 20% dispensing). The water motion was more irregular than the 1% w/v solution, and apparent aspirations occurred. Three water streams were observed in the front, middle, and back of the trachea, respectively, as shown by the dashed lines in Fig. 11a. This was consistent with the observations in the compete-throat model (Fig. 7a). The aspirations at the front, middle, and back of the trachea were caused by the epiglottis edge leak (off-edge flow), cuneiform tubercle recess overflow, and interarytenoid notch overflow, respectively. A further examination of the water motion recording confirmed the overflow via the cuneiform tubercle recesses that cause the lateral middle stream in the trachea.

Figure 11b illustrates the hydrodynamics of slow-dispensed liquids to the anterior oropharynx. In this case, no aspiration was observed for the 1% w/v MC solution. However, a water stream was observed in the dorsal trachea, which was verified to be the result of overflow via the cuneiform tubercle recesses, as illustrated by the pink line in Fig. 11b.

Aspiration quantification

Figure 12 shows the aspiration rate for water and 1% w/v MC solution under four dispensing conditions. Using the full-throat model in the study, it is observed that water, which is a thin liquid (Level 0), has one order of magnitude higher risk (9–20) for aspiration than the 1% w/v MC solution, which is a mildly thick liquid (Level 2). Among the four dispensing conditions, slow dispensing to the anterior oropharynx gives the highest aspiration risk, while slow dispensing to the posterior oropharynx gives the lowest risk, irrespective of the liquid consistency.

Figure 12
figure 12

Aspiration quantification for water and 1% w/v MC solution under varying dispensing conditions using the full-throat model.

Considering the dispensing site (i.e., tongue retraction) effects, dispensing liquids to the anterior oropharynx has significantly higher aspiration risks. The dispensing speed also has a significant impact on aspiration risks, regardless of the dispensing site or liquid type. However, different trends of the dispensing speed effects are observed depending on the dispensing site. To the anterior oropharynx, slow dispensing increases the aspiration, while to the posterior oropharynx, slow dispensing drastically decreases the aspiration, regardless of the liquid type (Fig. 11a,b).