Exploration of Pharyngeal Swallowing by Audiosignal Recording

M. Boiron,1 P. Rouleau,2 and E.H. Metman31Laboratoire de Physiologie, UFR Me´decine;2Service de Radiologie Adultes, Chru Bretonneau; and3Service de Gastroente´rologie,Chru Trousseau, Tours Cedex, France

Abstract. The aims of this study were to analyze thefollowing by audiorecording of swallows: (1) the influ-ence on the volume and consistency of ingested sub-stances on the audiosignal recorded during separateswallows; and (2) the characteristics of successive swal-lows during ingestion of 100 ml of the same substancesto define deglutitive behaviors. Volunteers followed twoprotocols. Protocol (P) 1 comprised ingestion of 100 mlof water or yoghurt in successive swallows and Protocol2 comprised separate swallows of different volumes ofthe same substances. Audiosignal recordings were madewith a dynamic microphone. The following parameterswere measured in P1: total time of ingestion (TT), num-ber of swallows necessary for ingestion (N), and spon-taneous swallowing intervals (SI). In P2 the duration (d)of each signal was measured according to consistencyand volume. Mean (m) values were then calculated(TTm, Nm, SIm, and dm). During P1, TTm for yoghurtwas significantly longer than for water (23.1 vs. 6.5 sec(men) and 21.8 vs. 7.8 sec (women). Nm was also greaterfor yoghurt (10.1 vs. 4.3 (men) and 10.0 vs. 4.8 (women).Three types of swallowing behavior were defined ac-cording to SI: swallowing at regular intervals (Reg) withincreasing intervals during ingestion (Prog) and swal-lowing at variable intervals (Irreg). These patterns didnot differ significantly according to sex. In P2 the in-crease in volume swallowed increased the duration (dm)of the signal for water (600 msec for 5 ml and 960 msecfor 15 ml). The dm for yoghurt was significantly lessthan for water (580 msec for 5 ml and 920 msec for 15ml). Our technique of recording sounds of pharyngealswallowing is simple, reproducible, and not expensive. Itpermitted the analysis of each swallow according to vol-ume and consistency and the determination of three

swallowing patterns (Reg, Prog, and Irreg), taking intoaccount the spontaneous swallowing interval. Ingestionby successive swallows could be used to characterizecertain pharyngoesophageal motor dysfunctioning in re-lation to this reference population and to integrate thisinto a deglutition rehabilitation program.

Key words: Pharynx — Audiosignal recording —Swallowing interval — Deglutitive behavior —Deglutition — Deglutition disorders.

Radiological and manometric techniques are often asso-ciated in order to analyze the pharyngeal phase of swal-lowing [1–4]. Scintigraphy [5,6] and the use of recentstrain gauges [7] have also contributed. However, suchmethods necessitate sophisticated and expensive equip-ment for the interpretation of results. The study of pha-ryngeal functioning has benefitted from another ap-proach based on auscultation and audiosignal recordingof swallowing [8–12], and current research emphasizesmethodological studies [13,14]. We have also used thistype of atraumatic technique to study mastication [15]. Inthe present study, we applied our technique for analyzingon the basis of sounds: (1) the influence of the volumeand consistency of ingested substances (water and yo-ghurt) on the signal recorded during separated swallows;and (2) the characteristics of successive swallows duringthe ingestion of 100 ml of the same substances to definedeglutitive behaviors.

Methods

Subjects and Procedure

The study was performed on 92 healthy volunteers (mean age 21.5 ±5.2 years, range 18–26 years, 56 women and 36 men) without history

Correspondence to:M. Boiron, Laboratoire de Physiologie, UFRMedecine, 37032 Tours Cedex, France

Dysphagia 12:86–92 (1997)

© Springer-Verlag New York Inc. 1997

of dysphagia, expressive speech impairment, or of oral or pharyngealsurgery. These subjects participated in two protocols: P1 (44 womenand 28 men) and P2 (12 women and 8 men).

The swallowing of two substances of different consistencies—mineral water and natural semiliquid yoghurt, was studied in the twoprotocols.

Protocol 1

At his or her own speed, each subject ingested 100 ml of water, 100 mlof yoghurt in random order at 5-min intervals while in a sitting position.The 100 ml of yoghurt corresponded to a weight of 125 g (viscosity4

190 cP). Both substances were at an ambient temperature.

Protocol 2

Each subject swallowed volumes of water and yoghurt measured bysyringe and placed in the mouth. Each volume was kept in the mouthand then swallowed. Volumes were of 3, 5, 8, 10, 15, and 20 ml; eachswallowed twice at 1-min intervals in random order. Ingestion of thetwo substances was separated by 5 min.

Sound recordings for each protocol were made with a smallsurface (1 cm2), commonly available dynamic microphone (Electret tieclip microphone Monacor ECM-2005 (Taiwan); frequency range 50–16,000 Hz) placed in direct contact with the skin, on the antero-lateralsurface of the neck pressing on the trachea just below the cricoidcartilage. It was oriented to perceive motions in the axial plane andadjusted to avoid interference from sound produced by the carotid pulseand raising the larynx. The microphone was kept in place by a fabriccollar and the subject was not permitted to move his head duringswallowing. The audiosignal was directly transcribed graphically (Al-var recorder, Paris, France) and recorded simultaneously with a Tech-nics cassette tape recorder RS-BX404 (Osaka, Japan) connected to aPioneer amplifier A-227 (Tokyo, Japan). Each recording was subse-quently analyzed after integration.

Analysis of Recordings

Protocol P1

The following parameters were recorded for each ingestion of 100 mlof water or yoghurt: number of swallows (N), total time (sec) of in-gestion (TT), and spontaneous swallowing interval (SI) (sec) separatingeach deglutition. TT corresponds to the time from the first to the lastswallow. Mean values (Nm ± SD), (TTm ± SD), and (SIm ± SD) werecalculated for men and women.

For each subject and each substance, a pattern of deglutitivebehavior was established on a graph with the successive intervals onthe abscissa and the corresponding spontaneous SI in sec on the ordi-nate. Subjects were divided into three patterns of swallowing on thebasis of analysis of individual patterns for swallowing yoghurt (whichcomprised the greatest number of swallows): (1) regular pattern (Reg)in which the intervals between successive swallows were equal orvaried by less than 10% from the mean of the first two intervals; (2)progressive pattern (Prog) with intervals increasing through ingestion(with lengthening of more than 10% of the preceding interval) or pro-gression by stages of not more than four equal intervals; and (3) ir-regular pattern (Irreg). In view of the good agreement (80%) betweeningestion of yoghurt and water, the distribution of subjects into Reg,Prog, and Irreg was not changed for analysis of ingestion of water.

Protocol P2

The maximum duration (d) and sound amplitude (a) of each swallowwere measured for each volume swallowed and for each substance.Mean duration (dm ± SD) and sound amplitude (am ± SD) were cal-culated for each volume and each substance for all subjects (Table 1).

Reproducibility Study

Reproducibility 1

Ten subjects in P1 took part for a second time 2 days later.

Table 1. Swallowing audiosignal. Variation of mean duration of signal (dm ± SD in ms) according to volume ingested (V in ml) for water and yoghurt

V 3 ml 5 ml 8 ml 10 ml 15 ml 20 ml

Water 600± 46 650± 80 690± 90 850± 62 960± 60 990± 52n 4 20 (610± 70) 660± 80) (660± 80) (920± 70) (1,000± 75) (1,000± 70)

NS NS S S NS

S S

S

Yoghurt 540± 65a 580± 60a 620± 80a 760± 70a 880± 90a 920± 60a

n 4 20 (510± 80) (520± 80) (630± 70) (710± 70) (850± 80) (890± 50)

NS NS S S NS

S S

S

aSignificantly different values (p < 0.01) compared with values measured for water.( ) Values for the second swallow for each volume (reproducibility 1).NS 4 values not significantly different; S4 significantly different values (p < 0.01).

M. Boiron et al.: Swallowing Behaviors and Sounds 87

Reproducibility 2

In P2, all volumes were ingested twice and dm of the second volumewere therefore compared to dm of the first.

Reproducibility 3

Ten subjects from P2 twice ingested 5 and 15 ml of water and yoghurtat a 2-day interval in random order.

Statistical Analysis

Student’st test and Spearman’s test for small cohorts were used tocompare the results. Thex2 test was used to compare swallowingbehaviors between men and women. Correlation tests were used for thereproducibility studies.

Results

Protocol 1—Deglutitive Behavior

Figure 1 shows an example of a typical audiorecordingof ingestion of 100 ml water and 100 ml yoghurt.

The TTm ingestion times were significantlyhigher for yoghurt regardless of sex: 23.1 ± 8.1 sec vs.6.5 ± 3.0 sec,p < 0.01 (men4 28) and 21.8 ± 7.8 sec vs.6.8 ± 3.2 sec,p < 0.01 (women4 44). Significant dif-ferences were also found for the number of swallowsaccording to consistency, the Nm for yoghurt beinggreater than that for water: 10.1 ± 2.9 vs. 4.3 ± 2.0,p <0.01 (men4 28); and 10.0 ± 2.9 vs. 4.8 ± 1.5,p < 0.01(women 4 44), respectively. However, TTm and Nmremained comparable between men and women for thesame substance.

Histograms of distribution of subjects accordingto N (Fig. 2) revealed that 43% of men swallowed thewater in 3 swallows whereas 51% of women required 4to 5 swallows. For yoghurt 35% of men and 30% ofwomen required 8–9 swallows. However, for 23% ofmen a small number of swallows (4–5) was sufficient.

Histograms of distribution of subjects according

to TT (Fig. 3) showed similarity in swallowing time formen and women for water, with a maximum of subjects(nearly 40%) completing swallowing in 5–7 sec. For35%–37% of subjects (men and women), yoghurt wasswallowed in 15–20 sec.

Patterns of yoghurt swallowing behavior were es-tablished for each subject and the distribution of the 72subjects was as follows: Reg4 22% men, 16% women;Prog4 26% men, 41% women; and Irreg4 52% men,43% women. However, the type of deglutitive behaviordid not seem to be statistically related to sex (x2 4 1.18).Figure 4 shows three examples of individual patterns(Reg, Prog, and Irreg) for water and yoghurt and meanpatterns for all 72 subjects. It can be seen that 80% ofsubjects had similar deglutitive behavior for water andyoghurt. These similarities are shown in Figure 4 asmean patterns.

Swallowing interval (SI) for water varied from0.8 to 3.5 sec (SIm4 1.4 sec) for Reg, from 0.5 to 5.2sec (SIm4 1.9 sec) for Prog, and from 0.5 to 3.7 sec(SIm 4 1.4 sec) for Irreg. For yoghurt, the swallowingintervals were from 1.3 to 3.0 sec (SIm4 2.1 sec) forReg, from 1 to 5.7 sec (SIm4 2.8 sec) for Prog, andfrom 1.0 to 4.2 sec (SIm4 2.2 sec) for Irreg. Meanvalues of SI were always higher for yoghurt than forwater (Fig. 4).

Protocol 2—Swallowing Audiosignal: Effect of Volumeand Consistency

Amplitudes, expressed in mV, reflected the intensity ofsounds and depended on the position and interface of themicrophone. There was wide interindividual variabilityfor amplitude and no significant difference for volume orconsistency of each subject.

Influence of Volume

Signal duration dm increased significantly in relation tovolume for both water and yoghurt; dm from 600 to 990msec for water and from 540 to 920 msec for yoghurt and

Fig. 1. Examples of typical audiosignal recording of swallowing during ingestion of 100 ml water (upper tracing) and 100 ml semiliquid yoghurt(lower tracing) in the same subject. The total time of ingestion (TT) was shorter for water, with a small number of swallows, compared with yoghurt.

88 M. Boiron et al.: Swallowing Behaviors and Sounds

3 ml and 20 ml, respectively. These values were signifi-cantly different for two clear levels of volume for bothwater and yoghurt: levels of 3-5-8 ml and 10-15-20 ml.These values are shown in Table 1. Figure 5 shows atypical example of increase in duration for 4 signals re-corded for 1 subject during increasing volumes.

Influence of Consistency

Table 1 shows dm values in relation to consistency. Withyoghurt the values were significantly low for all volumes(p < 0.01) with a decrease of around 70 msec (60–150msec).

Reproducibility

Reproducibility 1

In P1, the swallowing patterns were unchanged. TT andN remained correlated for each subject.

Reproducibility 2

In P2, dm were not significantly different for deglutitionof the same volume performed at a 1-min interval (Ta-ble 1).

Reproducibility 3

In P3, dm was not significantly different during deglu-tition of 5 and 15 ml performed 2 days later. It was 640± 60 ml vs. 650 ± 70 ml for 5 ml water and 940 ± 60 ml

vs. 920 ± 70 ml for 15 ml with yoghurt. The values were570 ± 80 ml vs. 590 ± 70 ml for 5 ml and 850 ± 60 mlvs. 860 ± 50 ml for 15 ml. As we showed before, valuesfor yoghurt were significantly lower.

Discussion

Our audiosignal recording and analysis techniques dur-ing swallowing are simple and noninvasive. They requireonly a commonly available microphone, a tape recorder,and a recorder to transcribe the signal in real time and fordifferential analysis. This method is reproducible forboth the analysis of separate swallows and for analysis ofswallowing behavior. The quality of our recordings de-pended on placing of the microphone near the cricoidcartilage and its orientation in the direction of theesophagus. This position was considered by Takahashi etal. [14] as optimal. They explored 24 sites in the neckand retained only 3 close to the cricoid. The sounds thatwe recorded were decoded by Hamlet et al. [11] whoattributed them to the passage of a bolus at the level ofthe cricopharyngeal canal. They emphasized that onlyvariations in speed caused sounds. However, they con-sidered that movements such as raising the larynx andmoving the epiglottis also make up part of the signal. Thecricopharyngeal muscle, which is responsible for closingthe upper esophageal sphincter (UES), is certainly themost important muscle of this sphincter which moreovercomprises other structures involved in its closing andopening [11,16–18]. It has been shown that opening de-

Fig. 3. Histogram of distribution of men and women according to totaltime of ingestion (TT) for the ingestion of 100 ml of water and 100 mlof yoghurt. Top: still mineral water; bottom: liquid yoghurt. Ingestionof yoghurt takes longer. A similarity can also be seen in the distributionof men and women for both substances.

Fig. 2. Histogram of distribution of men and women according tonumber of swallows (N) for the ingestion of 100 ml of water and 100ml of yoghurt. Top: still mineral water; bottom: semiliquid yoghurt.The ingestion of water and yoghurt requires more swallows in women.There is a similarity of distribution for yoghurt with a maximum ofsubjects requiring 8–9 swallows.

M. Boiron et al.: Swallowing Behaviors and Sounds 89

pends on the quantity of both the bolus and oropharyn-geal propulsion [2,20].

Our results showed that the duration of each sig-nal increased according to the volume swallowed, what-ever the consistency. Values of 600–990 msec for waterand 540–920 msec for yoghurt were only different fortwo volume levels: 3–8 ml and 10–20 ml. Durations ofthe same order corresponding to the opening of the UEShave been reported: 340–540 msec for volumes of 1–20ml of barium meal [17], 370 for swallowing saliva to 650msec for 20 ml of barium meal [19], and 900 msec for 5ml water [7]. Castell and Castell [20] also gave a relax-ation time of around 560 msec for 5 ml water and showedthat the greater the volume swallowed the greater thediameter and duration of the opening. Kahrilas et al. [2]added that adaptation of the diameter of the UES was theresult of the force of propulsion by the base of the tongueand that upstream peristalsis facilitated the clearing ofthe pharynx and played little part in the propulsion of thebolus.

Our results for yoghurt showed a reduction in theduration of the swallowing signal (around 70 msec) forall volumes compared with water. As shown by Robbinset al. [3], the duration of the opening of the UES wasgreater for liquids which spread across the pharynx,whereas substances with greater consistency pass morequickly through the UES and in a more compact manner.

In our study, the total time of ingestion (TTm)

increased with consistency (22 sec vs. 6.5 sec) as did thenumber (Nm) of swallows (10 vs. 4). Certain authorshave emphasized that the tongue and the pharynx act likea pump which propels water to the stomach at greatspeed whereas a more viscous bolus reaches halfwaydown the esophagus and is then evacuated by peristalsis[5,21]. Jacob et al. [19] and Dantas et al. [22] considerthat when the viscosity of a bolus increases, resistance topassage increases, resulting in a decrease in speed ofdisplacement of the bolus in the pharyngo-esophagealcanal. However, recent studies [6] have explained thatviscosity does not affect speed of displacement of thebolus in the pharynx.

We observed that ingestion of both substances bywomen required more swallows and a longer duration.Robbins et al. [3] demonstrated a greater duration ofopening of the UES in women using techniques associ-ating manometry and videoradiography. It is interestingto note this difference between women and men becauseour protocol was based on the ingestion of 100 ml ofsubstance with successive swallows at the subject’s ownspeed. This type of protocol has not, to our knowledge,been previously studied.

We defined three patterns of swallowing behav-ior (Reg, Prog, and Irreg) by taking into account theevolution of intervals between each swallow. It is im-portant to consider this parameter because good coordi-nation of pharyngo-esophageal motor sequences depends

Fig. 4. Patterns of swallowing behavior for ingestionof yoghurt (100 ml) and water (100 ml) according tospontaneous swallowing interval (SI) in sec. Left: threeexamples of individual patterns; upper right: regularpattern of 13 subjects; middle right: progressivepattern of 26 subjects; lower right: irregular pattern of33 subjects.

90 M. Boiron et al.: Swallowing Behaviors and Sounds

on it. A small number of subjects had the Reg pattern. Aregular interval seems to be optimal, probably related toswallowing of consistent volumes. Doty [23] and Roman[24] established that buccal and pharyngeal sensationinitiates the swallowing program. Intervals were moreand more spaced out in the Prog pattern, suggesting thatincrease in the interval in this pattern could facilitateesophageal clearance. Vanek and Diamant [25] demon-strated evidence of a reciprocal influence of two succes-sive swallows on esophageal peristalsis for short inter-vals, less than 4 sec, which could lead to motor dysfunc-tion. Ask and Tibbling [26] and Meyer et al. [27] showedthat the amplitude of distal esophageal peristalsis of asecond swallow at more than a 5-sec interval was inhib-ited, thus suggesting the presence of a refractory periodfor smooth muscle, varying from one subject to another,which can be detected up to an interval of 20 sec. Inter-vals in our study were around 1.5 sec for water and 2.5sec for yoghurt. Our population was young and it isknown that the swallowing rhythm diminishes with age[3]. It could thus be considered that during successiveswallows, resistance to passage increases and/or propel-ling forces diminish. However, coordination with respi-ration must also be taken into account [4,28]. Messagesfrom the suprabulbar control are superimposed on sen-sory information (mainly from esophageal wall) whichcould modify the sequence and interval of swallows. Wedid not measure each volume swallowed but volumes of25–30 ml for water and 10–15 ml for yoghurt could becalculated. The values for water are comparable to thoseof Adnerhill et al. [29] who measured each volume takenfreely from a cup during ingestion of a liquid, swallowsbeing separated and nonsuccessive as in our study. Theyfound a mean volume of 21 ml. A study is in progress(Boiron et al., unpublished) to quantify volumes inadlibitum ingestion. The Irreg pattern was more frequent inour subjects, which could indicate a swallowing programthat is constantly in adjustment according to the volumeingested, and including respiratory pauses. Dietary andingestion habits could have had an influence on thesepatterns. Our method, which quantifies the parameters ofa swallowing sequence (total time of ingestion (TT),number of swallows necessary for ingestion (N), spon-

taneous swallowing intervals (SI), swallowing behavior)will enable clinicians to have a more objective apprecia-tion of swallowing dysfunction [30]. It can also be usedto compare control subjects with dysphagic patients as itprovides quantifiable measurements of the differencesinvolved. Similarly, our method measures deglutitiondisorders and this can be used to observe progress duringrehabilitation [31].

Conclusion

Our technique for recording the sounds of pharyngealdeglutition is simple, reproducible, and inexpensive. Itpermitted the analysis of each swallow according to thevolume and consistency of two ingested substances. Thedetermination of three swallowing patterns (Reg, Prog,and Irreg) has not previously been described. It dependson the spontaneous interval noted between each swallowand is evidence therefore of an acquired or reflex behav-ior. Ingestion by successive swallows could be used totry to characterize certain types of primary or secondarypharyngo-esophageal motor dysfunction, e.g., postopera-tive, in relation to this reference population. Our methodcould be used in a deglutition rehabilitation program.

References

1. Cook IJ, Dodds WJ, Dantas RO, Kern MK, Massey BT, LangIM, Brasseur JG, Hogan WJ: Opening mechanisms of the upperesophageal sphincter.Am J Physiol 257:G748–G759, 1989

2. Kahrilas PJ, Logemann JA, Lin S, Ergun GA: Pharyngeal clear-ance during swallowing: a combined manometric and videofluo-roscopic study.Gastroenterology 103:128–136, 1992

3. Robbins J, Hamilton JW, Lof GI, Kempster GB: Oropharyngealswallowing in normal adults of different ages.Gastroenterology103:823–829, 1992

4. Maddock DJ, Gilbert RJ: Quantitative relationship between liq-uid bolus flow and laryngeal closure during deglutition.Am JPhysiol 265:G704–G711, 1993

5. Buthpitiya AG, Stroud D, Russell COH: Pharyngeal pump andesophageal transit.Dig Dis Sci 32:1244–1248, 1987

6. Kim CH, Hsu JJ, O’Connor MK, Weaver AL, Brown ML, Zins-meister AR: Effect of viscosity on oropharyngeal and esopha-geal emptying in man.Dig Dis Sci 39:189–192, 1994

7. Wilson JA, Pryde A, McIntyre CCA, Heading RC: Normal pha-ryngoesophageal motility. A study of 50 healthy subjects.DigDis Sci 34:1590–1599, 1989

8. Stott FD: The laryngeal microphone as an aid to treatment ofbulbar poliomyelitis.Br Med 20:1416, 1953

9. Logan WJ, Kavanagh JF, Wornall AW: Sonic correlates of hu-man deglutition.J Appl Physiol 23:279–284, 1967

10. Mackowiak RC, Brenman HS, Friedman MHF: Acoustic profileof deglutition.Proc Soc Exp Biol Med 125:1149–1152, 1967

11. Hamlet S, Nelson RJ, Patterson RL: Interpreting the sounds of

Fig. 5. Evolution of the duration of the typical swallowing audiosignalfor decreasing volumes, in the same subject.

M. Boiron et al.: Swallowing Behaviors and Sounds 91

swallowing: fluid flow through the cricopharyngeus.Ann OtolRhinol Laryngol 99:749–752, 1990

12. Lebel D, Parel CL, Thouvenot J: Exploration de la de´glutition apartir de son signal sonore.Arch Int Physiol Biochim 98:75–86,1990

13. Hamlet S, Penney DG, Formolo J: Stethoscope acoustics andcervical auscultation of swallowing.Dysphagia 9:63–68, 1994

14. Takahashi K, Groher ME, Michi K: Methodology for detectingswallowing sounds.Dysphagia 9:54–62, 1994

15. Boiron M, Lemaire MC, Unger G, Thouvenot J: Possibilite´d’exploration fonctionnelle de la mastication a` partir de signauxphoniques.Arch Int Physiol Bioch Biophys 101:399–403, 1993

16. Code CF, Schlegel JF: Motor action of the esophagus and itssphincters. In: Code CF (ed.):Handbook of Physiology,Sect 6:Alimentary Canal,Vol 4. Washington DC, American Physiologi-cal Society, 1821–1839, 1968

17. Kahrilas PJ, Dodds WJ, Dent J, Logemann JA, Shaker R: Upperesophageal sphincter function during deglutition.Gastroenter-ology 95:52–62, 1988

18. Lang IM, Shaker R: An update on the physiology of the com-ponents of the upper esophageal sphincter.Dysphagia9:229–232, 1994

19. Jacob P, Kahrilas PJ, Logemann JA, Shah V, Ha T: Upperesophageal sphincter opening and modulation during swallow-ing. Gastroenterology 97:1469–1478, 1989

20. Castell JA, Castell DO: Upper esophageal sphincter/pharyngealmanometry.Gullet 2:139–144, 1992

21. Fisher MA, Hendrix TR, Hunt JN, Murrills A: Relation betweenvolume swallowed and velocity of the bolus ejected from thepharynx into the esophagus.Gastroenterology 74:1238–1240,1978

22. Dantos RO, Kern MK, Massey BT, Dodds WJ, Kahrilas PJ,

Brasseur JG, Cook IL, Lang IM: Effect of swallowed bolusvariables on oral pharyngeal phases of swallowing.Am J Physiol258:G675–G681, 1990

23. Doty RW: Neural organization of deglutition. In: Code CF (ed.):Handbook of Physiology,Sect 6: Alimentary Canal.Vol 4.Washington DC, American Physiological Society, 1861–1902,1968

24. Roman C: Controˆle nerveux de la de´glutition et de la motricite´oesophagienne chez les mammife`res. J Physiol (Paris) 81:118–131, 1986

25. Vanek AW, Diamant NE: Responses of the human esophageusto paired swallows.Gastroenterology 92:643–650, 1987

26. Ask P, Tibbling L: Effect of interval between swallows onesophageal peristalsis.Am J Physiol 238:G485–G490, 1980

27. Meyer GW, Gerhardt DC, Castell DO: Human esophageal re-sponse to rapid swallowing: muscle refractory period or neuralinhibition. Am J Physiol 241:G129–G136, 1981

28. Shaker R, Li Q, Ren J, Townsend WF, Dodds WJ, Martin BJ,Kern MK, Rynders A: Coordination of deglutition and phase ofrespiration: effect of aging, tachypnea, bolus volume andchronic obstructive pulmonary disease.Am J Physiol 263:G750–G755, 1992

29. Adnerhill I, Ekberg O, Groher ME: Determining normal bolussize from thin liquids.Dysphagia 4:1–3, 1989

30. Logemann JA, Pauloski BR, Rademaker A, Cook B, Graner D,Milianti F, Beery Q, Stein D, Bowman J, Lazarus C, Heiser MA,Baker T: Impact of the diagnosis procedure on outcome mea-sures of swallowing rehabilitation in head and neck cancer pa-tients.Dysphagia 7:179–186, 1992

31. Bartolome G, Neumann S: Swallowing therapy in patients withneurological disorders causing cricopharyngeal dysfunction.Dysphagia 8:146–149, 1993

92 M. Boiron et al.: Swallowing Behaviors and Sounds