Acta Oto-Laryngologica
ISSN: 0001-6489 (Print) 1651-2251 (Online) Journal homepage: http://www.tandfonline.com/loi/ioto20
Biomechanics of the Human Epiglottis B. Raymond Fink, Roy W. Martin & Charles A. Rohrmann To cite this article: B. Raymond Fink, Roy W. Martin & Charles A. Rohrmann (1979) Biomechanics of the Human Epiglottis, Acta Oto-Laryngologica, 87:3-6, 554-559 To link to this article: http://dx.doi.org/10.3109/00016487909126464
Published online: 08 Jul 2009.
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Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ioto20 Download by: [University of California, San Diego]
Date: 12 February 2016, At: 14:30
Acta Otolaryngol87: 554-559, 1979 BIOMECHANICS OF THE HUMAN EPIGLOTTIS B. Raymond Fink, Roy W. Martin and Charles A. Rohrmann From the Departments of Anesthesiology and Radiology, University of Washington, Seattle, Washington, USA
Downloaded by [University of California, San Diego] at 14:30 12 February 2016
(Received July 17, 1978)
Abstract. The mechanism that folds the epiglottis down over the closed larynx in the course of swallowing has been unclear. Measurements of the force needed to fold the epiglottis in cadaver specimens exceed the estimated force available from the aryepiglottic muscle. Frame-byframe analysis of cinefluorograms reveals that deglutitional epiglottic downfolding occurs at the time of maximal elongation of the hyoepiglottic ligament. The observations lead us to propose a conical model of epiglottic downfolding which also explains the conical shape of the epiglottis usual in early infancy. The infant shape may be part of a protective partially closed entrance adaptive to suckling, while maturational widening of the opening adapts to the growing respiratory demands of increasing physical exertion.
Cineradiography has firmly established that the human epiglottis turns down backward over the top of the closed larynx in the course of normal deglutition (Rushmer & Hendron, 1951; Saunders et al., 1951; Ardran & Kemp, 1952; Ramsey et al., 1955). The protective value of this event is well understood: the downfolded epiglottis guides the bolus away from the laryngeal entrance and prevents any residue from fouling the cavity during re-establishment of the airway. The mechanism that causes the epiglottis to fold down, however, is still unclear. A push by the tongue, a push by the swallowed bolus, a pull by the aryepiglottic muscles, all can and have been incriminated. But it is well known that the downfolding also occurs in a dry swallow, and that the aryepiglottic muscle often contracts without downfolding the epiglottis at all, for example, in phonation. In this report we show that analysis of the events by cineradiography and measurements of the epiglottic folding force in fresh cadaver Acta Otolciwngol87
specimens point to the existence of a previously unrecognized factor in the mechanics of deglutitional epiglottic downfolding. METHODS Standard clinical cinefluorography was employed to time the downfolding of the epiglottis in relation to the passage of a swallowed radiopaque bolus and other laryngeal changes. Lateral and anteroposterior 16 mm black and white motion pictures were filmed at the rate of 24-32 frames per sec in the course of routine examination of five adult patients requiring investigation of the upper alimentary tract. The examinations revealed no structural abnormality in this region. The developed motion pictures were projected at various speeds or in ‘stopped motion’. All measurements were made on the projected image at the same magnification. The force necessary to fold the epiglottis down to a horizontal configuration was measured in fresh cadaver specimens of 4 adult and 11 infant larynges. The larynx as a whole was immobilized by mounting the cricoid cartilage on a three-piece chuck and clamping the posterior borders of the laminae of the thyroid cartilage. To depress the epiglottis a rod incorporating a force transducer and mounted on a micromanipulator was placed against the anterosuperior edge of the epiglottis- in the median line. The vertical distance moved by the rod and the force exerted on the epiglottis were recorded on the x and y axes of an xy recorder.
Biomechanics of the human epiglottis
20
I0
30
40
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FRAME NO
Fig. 1. Time course of changes in the distance between the body of the hyoid bone and the epiglottis during cinematography of deglutition. The distance was measured from the inferior borders of the body of the hyoid bone to the groove on the posterior surface of the epiglottic cartilage where the epiglottic tubercle and epiglottis proper meet. The short curved lines show the concomitant changes in the attitude of the epiglottis relative to the body of the hyoid bone, which is indicated by a vertical bar. All distances were measured in constant arbitrary units at constant magnification. The frames are numbered from the beginning of deglutitional ascent of the hyoid bone. The graphs begin at the commencement of ascent of the larynx toward the hyoid bone, and are from five adults.
RESULTS
Cineradiograp hy The motion pictures confirmed previous reports (e.g. Saunders et al., 1951) that in the course of the second stage of deglutition laryngeal closure is accompanied by upward and forward movement of the hyoid bone. The larynx was drawn toward the hyoid bone and the vocal and vestibular folds became folded and adducted and occluded the lumen. The lateral views demonstrated that elevation of the larynx toward the hyoid bone distorted the lower portion of the median thyrohyoid fold (Fink, 1976). The fold became considerably shortened vertically below the level of the hyo-epiglottic ligament and greatly elongated anteroposteriorly at the level of the ligament. The apparent effect was to push the hyoid bone forward and the epiglottic tubercle backward against the superomedial surface of the adducted aryepiglottic and vestibular folds. The attitude of the epiglottis was a function of the hyoepiglottic distance, as indicated in
555
Fig. 1 . The figure charts the hyo-epiglottic distance in successive frames, starting with the frame in which upward motion of the larynx began. Increase of this distance, signifying stretching of the hyo-epiglottic ligament, was accompanied by progressive downfolding of the epiglottis. Decrease of this distance at the end of the second stage was accompanied by rapid return of the normal upright attitude. As regards the attitude of the epiglottis (Fig. l), it can be seen that in every case downfolding of the epiglottis began suddenly at the instant of extreme anteroposterior elongation of the hyo-epiglottic ligament. The downfolding was completed in the course of 2 or 3 frames (0.06-0.09 sec) as previously noted by Saunders et al. (1951). The downfolding was also observable in the course of swallowing air, that is, independently of the presence of a liquid bolus or of backward pressure by the base of the tongue against the epiglottis. Return of the epiglottis to the upright, unfolded configuration was even more sudden than the downfolding and occurred at the beginning of descent and reopening of the larynx. The first event in the reopening sequence was always a reduction of the anteroposterior elongation at the level of the hyo-epiglottic ligament, which preceded the recoil of the epiglottis. In anteroposterior projection, the site of the downfolded epiglottis was defined by the layers of opaque bolus material above and below it (Fig. 2), and the process of downfolding could sometimes be followed in its entirety. It was noted that the surface of the epiglottis outlined by the bolus was not flat but distinctly conical.
Force data The force required to depress the epiglottis to a horizontal plane in autopsy specimens from 4 adults and 1 1 infants is listed in Table I. The complete set of measurements on one adult larynx is shown in Fig. 3. In the table there is a suggestion that the force increases with age, perhaps indicative of an increasing Acta Otola1yngol87
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B . R . Fink et al.
Fig. 2 . Frames from a cineradiographic study of deglutition. Anteroposterior projection. The base of the downfolded epiglottis is outlined by the opaque bolus on its upper and lower surfaces and appears as a transverse
arch. The upper surface is more sharply curved than the lower surface, and the curvature is more marked in the right hand picture B , taken two frames (0.06 second) later than the one on the left, A.
stiffness of the epiglottic cartilage. The average force required in adults was 16 g .
Table I. Foldingforcea on human epiglottis Sex
DISCUSSION The underlying mechanisms can be clarified by considering the hyoid bone to be suspended from the skull and mandible, and the larynx to be suspended from the hyoid bone (Fink, 1976). The hyo-laryngeal suspension consists primarily of the lateral thyrohyoid ligaments posteriolaterally and the median thyrohyoid fold anteromedially. The last-named structure, as recently described, is an important mechanical element of the primate larynx. It is composed of the epiglottic cartilage (in man, the epiglottis proper and the epiglottic tubercle), the hyo-epiglottic and thyro-epiglottic ligaments, the anterior thyrohyoid ligament, the intervening connective tissue, and the overlying mucosa. The bilateral soft tissue laryngeal folds (aryepiglottic, vestibular, vocal), the interarytenoid fold, and the median thyrohyoid Actu Otolunwgol87
Adults 1. 2. 3. 4.
6 0
6
P
Mean S.D.
Age (Y.)
Folding force (g)
24 37 62 85
6 11 22 25
52 27
16 9
Inf a n ts
0 P
6 0
Mean S.D.
0.03 0.08 1.5 1.6 2.3 2.5 2.7 3.5 4.2 4.1 4.4 5.7
2.2 1.8 1.8 1.3 3.6 4.8 3.0 1.9 1.6 4.0 0.5 2.2
2.7 1.8
2.4 1.2
Normal force applied to tip of anterior epiglottic surface, to depress epiglottis to the horizontal plane. S.D.: Standard Deviation.
a
Downloaded by [University of California, San Diego] at 14:30 12 February 2016
Biomechanics of the human epiglottis
557
stress to the model from the opposite side, at the site of attachment of the hyo-epiglottic ligament. This is done by grasping the paper ‘\ ‘ I lightly at the edges, below the level of the crease, whereupon the part above the crease, representing the epiglottis, immediately begins to fold down. Each limb of the crease functions as the directrix of a cone; the apex of the crease is the vertex of the cone. When the paper is gripped the directrices rotate towards each Fig. 3. Force-displacement behavior of the epiglottis. Data obtained by applying an external force ( F ) at the tip other and pull the attached paper after them, of the epiglottis ( X ) , in a freshly removed autopsy specigiving it a conical shape. men of the larynx immobilized at the cricoid and thyroid In the cineradiographs the limbs of the cartilages. groove are presumably set in motion by the bulging of the epiglottic tubercle. The tip of fold compose the folding-unfolding apparatus the tubercle functions as the vertex or axis of that regulates the size of the laryngeal lumen. rotation, and the limbs of the groove rotate In deglutitional closure, as distinct from effort toward each other and constrain the adjoining closure, the folding and occlusion are com- epliglottis to follow and thereby fold into a pleted by downfolding of the epiglottis. cone. The radiographic observations indicate that At this time the compression of the median at the peak of the deglutitional excursion of the thyrohyoid fold is also tilting the stem of the hyoid bone and the larynx the following cir- epiglottic cartilage, and indirectly pressing the cumstances prevail: downfolded epiglottis against the back of the (1) Forward translation of the hyoid bone in adducted arytenoids. Because of the elastic conjunction with extreme thyroid-hyoid ap- ligaments in the median thyrohyoid fold both proximation causes extreme elongation and tension on the hyo-epiglottic ligament at its attachment to the margins of the epiglottic tubercle. ( 2 ) The compression of the median thyrohyoid fold, secondary to extreme thyroidhyoid approximation, tends to make the epiglottic tubercle bulge backward transversely as well as vertically. The principle of the mechanism of folding A B C deduced from these observations is demonFig. 4 . Model of epiglottic folding: ( A ) Sketch of the posstrated in a working model that can be set up terior surface of the epiglottic cartilage to show the site in a few seconds. All that is needed is a rec- of the left half of the groove between the epiglottic tutangular piece of fairly stiff paper. The piece bercle below and the epiglottis proper above. ( B ) Paper of paper represents the complete epiglottic model creased to simulate the left and right halves of the groove between the “epiglottic tubercle” below and the cartilage (epiglottis and tubercle). A A-shaped “epiglottis proper” above. The concavity- of the crease crease is applied at the center (Fig. 4) to simu- faces the reader. At arrows the thumb and index grip the late the groove on the back of the cartilage, margins so as to increase the bulge of the tubercle. ( C ) Resulting deformation-the “epiglottis” has folded down between the epiglottic tubercle below and the towards the bulging “tubercle” and assumed a conical epiglottis proper above. One next applies shape. Actu Otolaryngol87
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the compression and downfolding are elastic. The epiglottis therefore automatically rebounded to its unfolded shape as soon as the compression relaxes. The suggested mechanism may be viewed as an adjuvant or partial substitute for the mechanisms usually invoked to downfold the epiglottis, such as pressure by the base of the tongue or by the swallowed bolus, or tension from the aryepiglottic muscles. Reasons for doubting the efficacy of the aryepiglottic muscle include the oblique angle at which these muscles approach the epiglottis and the small leverage available at their point of attachment. Our force measurements indicate that the aryepiglottic muscles would have to exert a total normal force of 16 g to downfold the epiglottis to the horizontal plane. Given the small cross-sectional area of each muscle, of the order of 2 mm2 by gross inspection, and estimating the maximal tensile stress generated by skeletal muscle as about 20 g per mm2, it appears that the aryepiglottic muscles are at best able to make only a limited contribution to the downfolding. This estimate is based on the fact that the direction of pull of the aryepiglottic muscle is not normal to the surface of the epiglottis but nearly parallel to it, and therefore the muscle operates at a mechanical disadvantage. In addition, the contractile force of a muscle decreases as the muscle shortens, so that the strength available from the aryepiglottic muscle becomes progressively less as the downfolding of the epiglottis progresses. The conical outline of the downfolded epiglottis observed in anteroposterior cineradiographs (Fig. 2) supports the idea that the mechanism in principle consists of transforming a flat sheet of tissue, i.e. (the unfolded epiglottic cartilage) into a cone. The conical configuration recalls the configuration of the infant epiglottis at rest. In effect, the adult larynx in the course of protective closure reverts transiently to the infantile configuration from which it developed. Conversely, the infantile resting configuration may be considAc 10 Otola, yngol87
ered a protective, already partly closed condition adaptive to the high frequency of swallowing in the suckling infant. Maturation of the infant larynx would then represent, in part, maturation toward a more open respiratory configuration at the entrance. It may be no coincidence that at the time of flattening of the epiglottis the incidence of crib death (Sudden Infant Death Syndrome) undergoes a marked diminution. Sasaki et al. have presented evidence of laryngeal maturation in support of such a view.
ACKNOWLEDGMENT This work has been supported by Grant HL19975 from the National Institutes of Health, United States Public Health Service.
ZUSAMMENFASSUNG Der Mechanismus, der den Kehlkopfdeckel wahrend des Schluckaktes uber den geschlossenen Larynx faltet, ist immer noch ungeklart. Die am Kadaver gemessene Biegungskraft der Epiglottis ist groRer als die des aryepiglottischen Muskels. Mit kinefluorographischen Untersuchungen wurde festgestellt, dal3 beim Schlucken die Kehlkopfdeckelumbiegung mit maximaler Ausdehnung des Ligamentum hyoepiglotticum einhergeht. Die Beobachtungen fuhren zur Annahrne eines kegelformigen Modelles der epiglottischen Umbiegung; ein solches Model1 wurde auch der konischen Form der Epiglottis im friihen Kindesalter entsprechen. Letztere stellt wahrscheinlich, im Dienst des Saugprozesses, einen Schutz fur den teilweise geschlossenen Glottiseingang dar. Mit fortschreitender Entwicklung enveitert sich der Glottiseingang, in Anpassung an den erhohten Atembedarf wahrend gesteigerter korperlicher Leistung.
REFERENCES Ardran, G. M. & Kemp, F. H . 1952. The protection of the laryngeal airway during swallowing. Br J Radio1 25, 406. Fink, B. R. 1975. The Human Larynx: A Functional Study, p. 94. Raven Press, New York." Fink, B. R. 1976. The median thyrohyoid fold: a nomenclatural suggestion. JAnatomy 122, 697. Ramsey, G. H . , Watson, J. S . , Gramiak, R. & Weinberg, S. A. 1955. Cinefluorographic analysis of the rnechanism of swallowing. Radiology 6 , 498.
Biomechanics of the human epiglottis
The mechanism of deglutition (second stage) as revealed by cineradiography. Ann Otol60, 897.
B . RayrnondFink, M.D. Dept. of Anesthesiology University of Washington Seattle, W A 98195, U S A
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Rushmer, R. F. & Hendron, R. A. 1951. The act of deglutition: a cinefluorographic study. J Appl Phvsiol3, 622. Sasaki, C. T., Levine, P. A , , Laitman, J. T. & Crelin, E. S . 1977. Postnatal descent of the epiglottis in man. Arch OtolaryngollO3, 169. Saunders, J. B . de C. M., Davis, C . & Miller, E. R. 1951.
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Actu Otoluryngol87
ISSN: 0001-6489 (Print) 1651-2251 (Online) Journal homepage: http://www.tandfonline.com/loi/ioto20
Biomechanics of the Human Epiglottis B. Raymond Fink, Roy W. Martin & Charles A. Rohrmann To cite this article: B. Raymond Fink, Roy W. Martin & Charles A. Rohrmann (1979) Biomechanics of the Human Epiglottis, Acta Oto-Laryngologica, 87:3-6, 554-559 To link to this article: http://dx.doi.org/10.3109/00016487909126464
Published online: 08 Jul 2009.
Submit your article to this journal
Article views: 17
View related articles
Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ioto20 Download by: [University of California, San Diego]
Date: 12 February 2016, At: 14:30
Acta Otolaryngol87: 554-559, 1979 BIOMECHANICS OF THE HUMAN EPIGLOTTIS B. Raymond Fink, Roy W. Martin and Charles A. Rohrmann From the Departments of Anesthesiology and Radiology, University of Washington, Seattle, Washington, USA
Downloaded by [University of California, San Diego] at 14:30 12 February 2016
(Received July 17, 1978)
Abstract. The mechanism that folds the epiglottis down over the closed larynx in the course of swallowing has been unclear. Measurements of the force needed to fold the epiglottis in cadaver specimens exceed the estimated force available from the aryepiglottic muscle. Frame-byframe analysis of cinefluorograms reveals that deglutitional epiglottic downfolding occurs at the time of maximal elongation of the hyoepiglottic ligament. The observations lead us to propose a conical model of epiglottic downfolding which also explains the conical shape of the epiglottis usual in early infancy. The infant shape may be part of a protective partially closed entrance adaptive to suckling, while maturational widening of the opening adapts to the growing respiratory demands of increasing physical exertion.
Cineradiography has firmly established that the human epiglottis turns down backward over the top of the closed larynx in the course of normal deglutition (Rushmer & Hendron, 1951; Saunders et al., 1951; Ardran & Kemp, 1952; Ramsey et al., 1955). The protective value of this event is well understood: the downfolded epiglottis guides the bolus away from the laryngeal entrance and prevents any residue from fouling the cavity during re-establishment of the airway. The mechanism that causes the epiglottis to fold down, however, is still unclear. A push by the tongue, a push by the swallowed bolus, a pull by the aryepiglottic muscles, all can and have been incriminated. But it is well known that the downfolding also occurs in a dry swallow, and that the aryepiglottic muscle often contracts without downfolding the epiglottis at all, for example, in phonation. In this report we show that analysis of the events by cineradiography and measurements of the epiglottic folding force in fresh cadaver Acta Otolciwngol87
specimens point to the existence of a previously unrecognized factor in the mechanics of deglutitional epiglottic downfolding. METHODS Standard clinical cinefluorography was employed to time the downfolding of the epiglottis in relation to the passage of a swallowed radiopaque bolus and other laryngeal changes. Lateral and anteroposterior 16 mm black and white motion pictures were filmed at the rate of 24-32 frames per sec in the course of routine examination of five adult patients requiring investigation of the upper alimentary tract. The examinations revealed no structural abnormality in this region. The developed motion pictures were projected at various speeds or in ‘stopped motion’. All measurements were made on the projected image at the same magnification. The force necessary to fold the epiglottis down to a horizontal configuration was measured in fresh cadaver specimens of 4 adult and 11 infant larynges. The larynx as a whole was immobilized by mounting the cricoid cartilage on a three-piece chuck and clamping the posterior borders of the laminae of the thyroid cartilage. To depress the epiglottis a rod incorporating a force transducer and mounted on a micromanipulator was placed against the anterosuperior edge of the epiglottis- in the median line. The vertical distance moved by the rod and the force exerted on the epiglottis were recorded on the x and y axes of an xy recorder.
Biomechanics of the human epiglottis
20
I0
30
40
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FRAME NO
Fig. 1. Time course of changes in the distance between the body of the hyoid bone and the epiglottis during cinematography of deglutition. The distance was measured from the inferior borders of the body of the hyoid bone to the groove on the posterior surface of the epiglottic cartilage where the epiglottic tubercle and epiglottis proper meet. The short curved lines show the concomitant changes in the attitude of the epiglottis relative to the body of the hyoid bone, which is indicated by a vertical bar. All distances were measured in constant arbitrary units at constant magnification. The frames are numbered from the beginning of deglutitional ascent of the hyoid bone. The graphs begin at the commencement of ascent of the larynx toward the hyoid bone, and are from five adults.
RESULTS
Cineradiograp hy The motion pictures confirmed previous reports (e.g. Saunders et al., 1951) that in the course of the second stage of deglutition laryngeal closure is accompanied by upward and forward movement of the hyoid bone. The larynx was drawn toward the hyoid bone and the vocal and vestibular folds became folded and adducted and occluded the lumen. The lateral views demonstrated that elevation of the larynx toward the hyoid bone distorted the lower portion of the median thyrohyoid fold (Fink, 1976). The fold became considerably shortened vertically below the level of the hyo-epiglottic ligament and greatly elongated anteroposteriorly at the level of the ligament. The apparent effect was to push the hyoid bone forward and the epiglottic tubercle backward against the superomedial surface of the adducted aryepiglottic and vestibular folds. The attitude of the epiglottis was a function of the hyoepiglottic distance, as indicated in
555
Fig. 1 . The figure charts the hyo-epiglottic distance in successive frames, starting with the frame in which upward motion of the larynx began. Increase of this distance, signifying stretching of the hyo-epiglottic ligament, was accompanied by progressive downfolding of the epiglottis. Decrease of this distance at the end of the second stage was accompanied by rapid return of the normal upright attitude. As regards the attitude of the epiglottis (Fig. l), it can be seen that in every case downfolding of the epiglottis began suddenly at the instant of extreme anteroposterior elongation of the hyo-epiglottic ligament. The downfolding was completed in the course of 2 or 3 frames (0.06-0.09 sec) as previously noted by Saunders et al. (1951). The downfolding was also observable in the course of swallowing air, that is, independently of the presence of a liquid bolus or of backward pressure by the base of the tongue against the epiglottis. Return of the epiglottis to the upright, unfolded configuration was even more sudden than the downfolding and occurred at the beginning of descent and reopening of the larynx. The first event in the reopening sequence was always a reduction of the anteroposterior elongation at the level of the hyo-epiglottic ligament, which preceded the recoil of the epiglottis. In anteroposterior projection, the site of the downfolded epiglottis was defined by the layers of opaque bolus material above and below it (Fig. 2), and the process of downfolding could sometimes be followed in its entirety. It was noted that the surface of the epiglottis outlined by the bolus was not flat but distinctly conical.
Force data The force required to depress the epiglottis to a horizontal plane in autopsy specimens from 4 adults and 1 1 infants is listed in Table I. The complete set of measurements on one adult larynx is shown in Fig. 3. In the table there is a suggestion that the force increases with age, perhaps indicative of an increasing Acta Otola1yngol87
Downloaded by [University of California, San Diego] at 14:30 12 February 2016
556
B . R . Fink et al.
Fig. 2 . Frames from a cineradiographic study of deglutition. Anteroposterior projection. The base of the downfolded epiglottis is outlined by the opaque bolus on its upper and lower surfaces and appears as a transverse
arch. The upper surface is more sharply curved than the lower surface, and the curvature is more marked in the right hand picture B , taken two frames (0.06 second) later than the one on the left, A.
stiffness of the epiglottic cartilage. The average force required in adults was 16 g .
Table I. Foldingforcea on human epiglottis Sex
DISCUSSION The underlying mechanisms can be clarified by considering the hyoid bone to be suspended from the skull and mandible, and the larynx to be suspended from the hyoid bone (Fink, 1976). The hyo-laryngeal suspension consists primarily of the lateral thyrohyoid ligaments posteriolaterally and the median thyrohyoid fold anteromedially. The last-named structure, as recently described, is an important mechanical element of the primate larynx. It is composed of the epiglottic cartilage (in man, the epiglottis proper and the epiglottic tubercle), the hyo-epiglottic and thyro-epiglottic ligaments, the anterior thyrohyoid ligament, the intervening connective tissue, and the overlying mucosa. The bilateral soft tissue laryngeal folds (aryepiglottic, vestibular, vocal), the interarytenoid fold, and the median thyrohyoid Actu Otolunwgol87
Adults 1. 2. 3. 4.
6 0
6
P
Mean S.D.
Age (Y.)
Folding force (g)
24 37 62 85
6 11 22 25
52 27
16 9
Inf a n ts
0 P
6 0
Mean S.D.
0.03 0.08 1.5 1.6 2.3 2.5 2.7 3.5 4.2 4.1 4.4 5.7
2.2 1.8 1.8 1.3 3.6 4.8 3.0 1.9 1.6 4.0 0.5 2.2
2.7 1.8
2.4 1.2
Normal force applied to tip of anterior epiglottic surface, to depress epiglottis to the horizontal plane. S.D.: Standard Deviation.
a
Downloaded by [University of California, San Diego] at 14:30 12 February 2016
Biomechanics of the human epiglottis
557
stress to the model from the opposite side, at the site of attachment of the hyo-epiglottic ligament. This is done by grasping the paper ‘\ ‘ I lightly at the edges, below the level of the crease, whereupon the part above the crease, representing the epiglottis, immediately begins to fold down. Each limb of the crease functions as the directrix of a cone; the apex of the crease is the vertex of the cone. When the paper is gripped the directrices rotate towards each Fig. 3. Force-displacement behavior of the epiglottis. Data obtained by applying an external force ( F ) at the tip other and pull the attached paper after them, of the epiglottis ( X ) , in a freshly removed autopsy specigiving it a conical shape. men of the larynx immobilized at the cricoid and thyroid In the cineradiographs the limbs of the cartilages. groove are presumably set in motion by the bulging of the epiglottic tubercle. The tip of fold compose the folding-unfolding apparatus the tubercle functions as the vertex or axis of that regulates the size of the laryngeal lumen. rotation, and the limbs of the groove rotate In deglutitional closure, as distinct from effort toward each other and constrain the adjoining closure, the folding and occlusion are com- epliglottis to follow and thereby fold into a pleted by downfolding of the epiglottis. cone. The radiographic observations indicate that At this time the compression of the median at the peak of the deglutitional excursion of the thyrohyoid fold is also tilting the stem of the hyoid bone and the larynx the following cir- epiglottic cartilage, and indirectly pressing the cumstances prevail: downfolded epiglottis against the back of the (1) Forward translation of the hyoid bone in adducted arytenoids. Because of the elastic conjunction with extreme thyroid-hyoid ap- ligaments in the median thyrohyoid fold both proximation causes extreme elongation and tension on the hyo-epiglottic ligament at its attachment to the margins of the epiglottic tubercle. ( 2 ) The compression of the median thyrohyoid fold, secondary to extreme thyroidhyoid approximation, tends to make the epiglottic tubercle bulge backward transversely as well as vertically. The principle of the mechanism of folding A B C deduced from these observations is demonFig. 4 . Model of epiglottic folding: ( A ) Sketch of the posstrated in a working model that can be set up terior surface of the epiglottic cartilage to show the site in a few seconds. All that is needed is a rec- of the left half of the groove between the epiglottic tutangular piece of fairly stiff paper. The piece bercle below and the epiglottis proper above. ( B ) Paper of paper represents the complete epiglottic model creased to simulate the left and right halves of the groove between the “epiglottic tubercle” below and the cartilage (epiglottis and tubercle). A A-shaped “epiglottis proper” above. The concavity- of the crease crease is applied at the center (Fig. 4) to simu- faces the reader. At arrows the thumb and index grip the late the groove on the back of the cartilage, margins so as to increase the bulge of the tubercle. ( C ) Resulting deformation-the “epiglottis” has folded down between the epiglottic tubercle below and the towards the bulging “tubercle” and assumed a conical epiglottis proper above. One next applies shape. Actu Otolaryngol87
Downloaded by [University of California, San Diego] at 14:30 12 February 2016
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the compression and downfolding are elastic. The epiglottis therefore automatically rebounded to its unfolded shape as soon as the compression relaxes. The suggested mechanism may be viewed as an adjuvant or partial substitute for the mechanisms usually invoked to downfold the epiglottis, such as pressure by the base of the tongue or by the swallowed bolus, or tension from the aryepiglottic muscles. Reasons for doubting the efficacy of the aryepiglottic muscle include the oblique angle at which these muscles approach the epiglottis and the small leverage available at their point of attachment. Our force measurements indicate that the aryepiglottic muscles would have to exert a total normal force of 16 g to downfold the epiglottis to the horizontal plane. Given the small cross-sectional area of each muscle, of the order of 2 mm2 by gross inspection, and estimating the maximal tensile stress generated by skeletal muscle as about 20 g per mm2, it appears that the aryepiglottic muscles are at best able to make only a limited contribution to the downfolding. This estimate is based on the fact that the direction of pull of the aryepiglottic muscle is not normal to the surface of the epiglottis but nearly parallel to it, and therefore the muscle operates at a mechanical disadvantage. In addition, the contractile force of a muscle decreases as the muscle shortens, so that the strength available from the aryepiglottic muscle becomes progressively less as the downfolding of the epiglottis progresses. The conical outline of the downfolded epiglottis observed in anteroposterior cineradiographs (Fig. 2) supports the idea that the mechanism in principle consists of transforming a flat sheet of tissue, i.e. (the unfolded epiglottic cartilage) into a cone. The conical configuration recalls the configuration of the infant epiglottis at rest. In effect, the adult larynx in the course of protective closure reverts transiently to the infantile configuration from which it developed. Conversely, the infantile resting configuration may be considAc 10 Otola, yngol87
ered a protective, already partly closed condition adaptive to the high frequency of swallowing in the suckling infant. Maturation of the infant larynx would then represent, in part, maturation toward a more open respiratory configuration at the entrance. It may be no coincidence that at the time of flattening of the epiglottis the incidence of crib death (Sudden Infant Death Syndrome) undergoes a marked diminution. Sasaki et al. have presented evidence of laryngeal maturation in support of such a view.
ACKNOWLEDGMENT This work has been supported by Grant HL19975 from the National Institutes of Health, United States Public Health Service.
ZUSAMMENFASSUNG Der Mechanismus, der den Kehlkopfdeckel wahrend des Schluckaktes uber den geschlossenen Larynx faltet, ist immer noch ungeklart. Die am Kadaver gemessene Biegungskraft der Epiglottis ist groRer als die des aryepiglottischen Muskels. Mit kinefluorographischen Untersuchungen wurde festgestellt, dal3 beim Schlucken die Kehlkopfdeckelumbiegung mit maximaler Ausdehnung des Ligamentum hyoepiglotticum einhergeht. Die Beobachtungen fuhren zur Annahrne eines kegelformigen Modelles der epiglottischen Umbiegung; ein solches Model1 wurde auch der konischen Form der Epiglottis im friihen Kindesalter entsprechen. Letztere stellt wahrscheinlich, im Dienst des Saugprozesses, einen Schutz fur den teilweise geschlossenen Glottiseingang dar. Mit fortschreitender Entwicklung enveitert sich der Glottiseingang, in Anpassung an den erhohten Atembedarf wahrend gesteigerter korperlicher Leistung.
REFERENCES Ardran, G. M. & Kemp, F. H . 1952. The protection of the laryngeal airway during swallowing. Br J Radio1 25, 406. Fink, B. R. 1975. The Human Larynx: A Functional Study, p. 94. Raven Press, New York." Fink, B. R. 1976. The median thyrohyoid fold: a nomenclatural suggestion. JAnatomy 122, 697. Ramsey, G. H . , Watson, J. S . , Gramiak, R. & Weinberg, S. A. 1955. Cinefluorographic analysis of the rnechanism of swallowing. Radiology 6 , 498.
Biomechanics of the human epiglottis
The mechanism of deglutition (second stage) as revealed by cineradiography. Ann Otol60, 897.
B . RayrnondFink, M.D. Dept. of Anesthesiology University of Washington Seattle, W A 98195, U S A
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Rushmer, R. F. & Hendron, R. A. 1951. The act of deglutition: a cinefluorographic study. J Appl Phvsiol3, 622. Sasaki, C. T., Levine, P. A , , Laitman, J. T. & Crelin, E. S . 1977. Postnatal descent of the epiglottis in man. Arch OtolaryngollO3, 169. Saunders, J. B . de C. M., Davis, C . & Miller, E. R. 1951.
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