Acta Otolaryngol (Stockh) 1992; 112: 816-823
The Middle Ear as a Baroreceptor T. J. ROCKLEY‘ and W. M. HAWKE* From the ‘Department of Otolaryngology, Enrt Birmingham Hospital, Bordesley Green f i t , Birmingham, West MidlandF 3 9 5ST, UK and the 2Departments of Otolaryngology and Pathology, Unwersity of Toronto, Ontario, Canada
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Rockley TJ, Hawke WM. The middle ear as a baroreceptor. Acta Otolaryngol (Stockh) 1992; 112 816-823. Underpressure in the middle ear is thought to be important in the pathogenesis of chronic otitis media with effusion and its sequelae, but the cause of the underpressure and the mechanisms responsible for regulation of the normal middle ear pressure are a matter of debate. Numerous studies have examined the effect of large pressure changes on the ear; however, the ear’s sensitivity to smaller pressure changes has received little attention. This study examines the sensitivity of the ear to atmosphericair pressure changes induced in the external ear canal. It is concluded that the normal ear is a very sensitive pressure receptor, and that the sensation is probably registered by stretch receptors in the tympanic membrane. Pathological changes in the tympanic membrane are associated with impaired baroreceptor function. The implications of these findings in the physiology of the ear and the regulation of middle ear presssure are discussed. Key words: middle ear pressure, tympanic membrane, stretch receptors, pressure receptors.
INTRODUCTION In the healthy ear, the gas pressure within the closed middle ear space is maintained close to atmospheric (1,2, 3). The origin of the abnormally low intratympanic pressures in middle ear disease states is at present controversial: it has been suggested (4) that the underpressure may arise suddenly from voluntary middle ear evacuation in patients with an abnormally patulous eustachian tube (the “sniffing theory”). The negative pressure may also arise more slowly from gas diffusion from the middle ear into the mucosa associated with deficient eustachian tube opening (S), or from a hydraulic effect of ciliary traction on middle ear mucus as it passes down the eustachian tube (6). The importance of understanding the physiology and pathophysiology of intratympanic pressure is evident, but at present the regulation of gas pressure in the normal ear is poorly understood. Pressure of gas within the middle ear is dependent on several factors; the composition of the gas, diffusion in and out of the mucosa, equilibration with the nasopharynx via opening of the eustachian tube, and active inflation or evacuation (e.g. by sniffing, noseblowing, or Valsalva’s manoeuvre). Chemoreceptive reflexes have been postulated (7) as a means of regulating middle ear pressure. The presence of chemoreceptor or glomus tissue in the middle ear mucosa has led to the suggestion that it may respond to gas composition changes in the middle ear, initiating “middle ear ventilation reflexes”, effected by the eustachian tube muscles. We have argued, however, that this is unlikely (8). Anatomically, glomus tissue has an angiochemoreceptor structure and is only inconstantly present in the middle ear mucosa. Very little attention has been paid to the phenomenon of baroreception in the middle ear and to the possible role pressure sensation might have in the regulation of middle ear pressure. This is in contrast to the considerable study that has been done (9) on the middle ear’s response to the large pressure variations that may occur in aeroplane fight and deep sea diving (causing such diseases as barotrauma, perilymph fistula, and alternobaric vertigo),
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Acta Otolaryngol (Stockh) I12
The middle ear ar a baroreceptor
and also to the tiny pressure vibrations that are sound waves (10). It is a matter of common experience that slight atmospheric pressure changes (for example those encountered when travelling in a train or car), or middle ear pressure changes (for example after blowing the nose), are registered in the ears causing a sensation of “fulness” and leading to a desire to “clear” the ears and re-equilibrate middle ear pressure. This sensation is an important consideration in the design of modern passenger transportation ( 1 1): air-pressure fluctuations in the carriages of high-speed trains must be kept to a level that is comfortable to passengers’ ears. This phenomenon is perhaps not surprising when one realises that the closed middle ear space is probably the only organ in the body that is structured as an air baroreceptor or pressure transducer. There is therefore the theoretical potential for baroreception in the ear, but this subject has thus far received little attention. The purpose of this study is to investigate the sensitivity of the ear to atmospheric pressure changes in both normal and pathological conditions; such information could provide some insight into the role of baroreception in the regulation of normal middle ear pressure, and how this system might fail in disease, resulting in middle ear underpressure.
MATERIAL AND METHOD Normal ears
Four experiments were performed on 28 volunteers (56 ears), aged between 19 and 50 years, with no history of chronic middle ear disease, and normal tympanic membranes at otomicroscopy. Each ear was tested separately using an impedance bridge apparatus (Peters AP67). This instrument, normally used for performing tympanometry, was modified by switching off the test tone, and after obtaining a comfortable airtight seal in the ear canal, the air pressure within the canal could be altered from -300 to +300mmH,O, the exact pressure being recorded on the instrument’s manometer. Adequacy of airtight seal was checked before and after each experiment by confirming that there was no variation in the manometer reading during induced static pressure changes. With this arrangement, several experiments were performed. To determine the subjective threshold of baroreception, the ear canal air pressure was increased or decreased from atmospheric at a constant rate of 50 mmH,O (50 decapascals) per 5 s. Subjects were asked to indicate the point at which they were first able to appreciate the change of pressure. The pressure level at which the subject responded on two out of three consecutive occasions was recorded as the threshold. Positive and negative pressure were tested separately. Adaptation of the pressure sensution. A positive pressure of 50 mmH,O above threshold was introduced into the ear canal and maintained for 3min. The subject was asked to indicate during that time period the point at which he or she was no longer aware of the sensation of pressure, thus providing an indication of physiological adaptation of the sensation. Specifirfty of the response. To determine whether the ear could distinguish between positive and negative pressure as a sensation, subjects were presented five times with pressures in the ear canal at 50mmH,O above threshold, either positive or negative, and asked to say whether they thought the pressure was positive or negative. Effect of iontophoresis. Subjective thresholds of baroreception in five subjects were retested after anaesthetising the tympanic membrane with a 2% lignocaine/l:2OOO adrenaline solution, using the technique of iontophoresis (12).
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Abnormal ears Thresholds to positive pressure change induced in the ear canal as described above were determined for 39 ears with otoscopically abnormal tympanic membranes (in 28 adult patients) without middle ear effusion or otorrhoea, attending an otologcal outpatient clinic. The abnormalities, which are regarded as long-term sequelae of otitis media with effusion (1) (listed below), were categorised as being either “minor” or “major”. To avoid possible tympanic membrane perforation in this group, some of whom had very atrophic membranes, pressure changes were limited to those encountered in routine tympanometry, i.e. a maximum of +200 mmH,O. Minor abnormalities (26 ears). Isolated patch of tympanosclerosis and atrophic segment of pars tensa were seen as well as retraction of the pars flaccida with adhesion to the neck of malleus; but without erosion of the notch of Rivinus, and with the depths of the retraction being fully visible otoscopically. Moreover, retraction of the posterior segment of the pars tensa, with adhesion to the incudostapedial joint, but with the depths of the retraction being fully visible otoscopically. Major abnormaliries (13 ears). Tympanosclerosisor atrophy affecting more than half of the pars tensa was noted as well as deep retraction of the pars flaccida, the full extent of the retraction not apparent on otoscopy, with or without erosion of the notch of Rivinus (but without cholesteatoma formation). Deep retraction of the posterior segment of the pars tensa into the sinus facialis or sinus tympani was also seen and a combination of the above abnormalities.
RESULTS Buroreception thresholds (see Fig. 1). This graph shows the range of subjective thresholds to pressure changes in the 56 normal ears tested. It was noted during testing that once an individual became familiar with the sensation, responses to positive pressure became very
HEOATWE PRESSURE
-lo
POMlVE PRESSURE mnlH*O
Fig. I. Thresholds of subjective sensitivity to pressure change in the ear canal, as found in 56 normal ears.
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Acta Otolaryngol (Stockh) 112
consistent for that individual, usually within 25 mmH,O of each other on repeat testing. Responses to negative pressure were more variable and less precise than for positive pressure. The responses to positive pressure in the ear canal are, however, more relevant to the clinical situation, as the tympanic membrane is displaced medially, simulating retraction. It may be seen that although there is variation between individuals in the subjective thresholds, the majority of people responded to pressures of less than 100 mmH,O. Adaptation (see Fig. 2). In all but one of the ears tested, the sensation of “fulness” in the ear was lost during the 3 min of the test despite the pressure in the ear canal being sustained, indicating that sensory adaptation takes place.
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+
Fig. 2. Adaptation of the pressure sensation. This graph shows the number of individuals who remained subjectively aware of a sustained positive pressure during a 3-minute test period (25 normal subjects, ears tested separately).
Minutes NUYEER
0
25
50
75
100
125
150
175
200
-200
PoSmvE PRESSURE rnrnH 0
Fig. 3. Threshold of subjective sensitivity to pressure change in the ear canal, as found in 39 abnormal ears.
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Table I. Baroreception thresholds before and a f e r iontophoresis
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Subject 1 Subject 2 Subject 3 Subject 4 Subject 5
Thresholds (mmH,O)
Thresholds after iontophoresis (mmH20)
- 100
None obtained from -300 to f 3 0 0 None obtained from -300 to +300 -200 +200 -225 + 300 -200None obtained to +300
- 150
+50 t75
- 100 -75
+ 130
- 125
i75
i-60
Specificity of discrimination between positiw and negatiue pressure. None of the subjects tested were able to distinguish subjectively between positive and negative pressure in the ear canal. The effect of iontophoresis (see Table I). In the 5 subjects whose thresholds to positive and negative pressure were retested after lignocaine iontophoresis, the ear became less sensitive to pressure change as a result of the local anaesthesia, as seen in Table I. Baroreception threshold in diseased ears (see Fig. 3 ) . Subjects with abnormalities of the tympanic membrane had impaired sensation to pressure change, as may be seen if Fig. 3 is compared with the distribution of baroreception thresholds for positive pressure in normal ears (Fig. 1). Statistical comparison of the results between the two groups (Mantel-Haenzel test) shows that this difference is significant: Chi-squared = 16.4, 1 degree of freedom; p < 0.001 (13). In general, more Severe tympanic membrane abnormalities were associated with less sensitive ears: for 10 ears tested, no threshold could be obtained within the test range of 0-200 mmH,O.
DISCUSSION The ear as a baroreceptor. It would appear from these results that the healthy ear is a Sensitive baroreceptor to air pressure changes induced in the ear canal, the threshold of sensitivity (for positive pressure) in most of the subjects tested being within the “normal range” of middle ear pressure accepted for tympanometry readings. Inducing a negative pressure in the ear canal gave more variable responses, possibly because it caused some venous filling and hence a volume change in the ear canal skin and pars flaccida, mitigating tympanic membrane displacement. To give some perspective on the ear’s sensitivity, Fig. 4
1.-12
Fig. 4. Displacement of the tympanic membrane in response to induced air-pressure changes. AP = Static air-pressure in the external ear canal AVtm = induced volume change in the position of the tympanic membrane. (Redrawn from (14) with permission of the Editor of Acta Otolaryngologica).
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The middle ear as a baroreceptor
shows the volume displacement of the tympanic membrane in response to induced pressure changes in the ear canal (14). As already noted, most subjects were aware of pressure changes of less than 100 mmH,O, and this corresponds to a volume displacement of the TM of less than 15 pl. Considering that on average the volume of the middle ear and mastoid air cells, is 6 OW p1 ( 15), it can be seen that the ear thus may be sensitive to changes of a fraction of one percent of that volume. It seems likely from experiment 2, however, that this sensitivity is only for rapidly occurring pressure changes, because sensory adaptation takes place; and therefore slowly occurring changes in middle ear pressure relative to the atmosphere are probably not registered by this baroreceptor mechanism. This study is of practical relevance when one considers that passenger ear discomfort is an important factor in the design of modem railways, including the new Channel Tunnel rail link between England and France (1 1). High-speed trains cause air-pressure changes when they enter tunnels, and the resulting ear sensation is distressing to some passengers. The anatomical site of baroreception. When the air pressure in the ear canal is altered, movement occurs in the tympanic membrane, ossicular chain, tympanic muscles, and labyrinthine window membranes ( 16). The baroreception sensation could conceivably be registered by distortion of the malleoincudal joint or tensor tympani tendon, as both of these have been shown to play an important role in the mechanics of the middle ear, limiting hydraulic damage to the labyrinth when the malleus is displaced. The lack of discrimination noted in our study between positive and negative pressure, and the diminished sensitivity after iontophoresis, suggest that the tympanic membrane itself is the origin of the barorecep tion sensation. This idea, that the tympanic membrane is somehow involved with middle ear pressure regulation, is not new. Schrapnell, over 150 years ago, in his classic description of the tympanic membrane (17) suggested different roles for the two parts: the pars tensa was relatively stiff and functioned primarily for sound conduction, while the pars flaccida was displaced more easily and accommodated pressure fluctuations. Stenfors et al. in 1979 (18) supported this concept in their experiments on pressure-induced displacement of the pars flaccida of rats, but later (3), realising that the volumes of gas that might be accommodated by this mechanism were relatively insignificant, proposed that the pars flaccida was actually a sensor mechanism for pressure fluctuations in the middle ear. This is an attractive idea, particularly since the pars flaccida does not seem to have the demonstrable role in sound transmission (19). The pars flaccida contains elastin fibres while the pars tensa does not (20); this arrangement echoes the structure of the arterial baroreceptor in the carotid sinus, whose wall is more elastic and distensible than the adjacent carotid artery. At present, it is not known whether stretch receptors exist within the tympanic membrane. Saunders & Weider (21), in their study entitled “Tympanic membrane sensation”, described it as apparently exclusively a nociceptive system. It may be that the specialised nerve endings in the pars tensa described originally by Wilson (22) in 1911 as “modified pacinian corpuscles” and rediscovered recently by Nagai & Tono (23) might be sensitive to tympanic membrane displacement (as suggested by Nagai & Tono), but this remains to be elucidated. We are currently undertaking studies on whole-mount cadaver tympanic membrane preparations to look at the distribution of these encapsulated endings in the pars tensa and flaccida. Baroreception in middle ear physiology and pathophysiology. As a result of our experiments, we would suggest the following role for baroreception in the non-auditory physiology of the ear. It seems to register short-term changes in middle ear pressure relative to atmospheric pressure in the conscious subject, the sort of pressure changes that might be caused by activity, e.g. sneezing, valsalva, sniffing or nose-blowing; leading to voluntary tubal opening and pressure equilibration by swallowing or yawning. It is interesting to note that the volume of air that may pass up the eustachian tube to the ear by tubal opening during a swallow is
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Ac- ~ o ~ g(Stockh) o l 112
approximately I5 PI ( 14); the same volume change that would cause a feeling of “fulness in the ear” for most subjects in our study. This protective mechanism would prevent damage to the tympanic membrane from excessive mechanical distortion, and also allow the sound conduction mechanism of the ear to function optimally. Slower middle ear pressure changes, for example from diffusion of gas into and out of the middle ear mucosa, are probably not consciously registered; but these changes are equilibrated easily by the frequent swallowing actions that occur normally throughout the day (average 10 per hour) in response to saliva in the pharynx (24), and which open the eustachian tube. Finally, we may speculate on the role of the middle ear baroreceptor mechanism in disease states characterised by intratympanic underpressure. Studies performed by Magnuson and his coworkers (4) have demonstrated that negative middle ear pressure may be induced suddenly by sniffing in certain individuals who suffer from the symptoms of intermittent patulous eustachian tube. This voluntary evacuation of the ear causes “locking” of the tube, thereby eliminating troublesome autophony. If repeated over a long time, middle ear atelectasis and cholesteatoma may ensure. From our studies, it would seem possible that the initial discomfort experienced by such individuals resulting from sudden evacuation of the ear would soon diminish as adaptation takes place, and retraction pocket formation would be accompanied by a further impairment of pressure application, allowing more damage to occur. Negative pressure may, however, develop in the middle ear more slowly. Sad6 & Luntz ( 5 ) showed gradual retraction of the tympanic membrane to its original position over 60min following air politzerisation of an atelectatic ear, due to diffusion of gas into the middle ear mucosa. In an experiment on cats, Murphy (6) demonstrated that mucus introduced into the middle ear was slowly cleared by ciliary action down the eustachian tube, and this was associated with the development of negative pressure in the ear caused by a hydraulic effect of the moving mucus column. We would suggest that slowly developing underpressures such as these would not cause symptoms in the ear, again because of adaptation of the sensation of pressure change, and therefore voluntary attempts to re-equilibrate the ears would not be made. Impaired baroreceptor function may play a part in the pathogenesis of retraction pockets of the tympanic membrane: it appears from our study that a damaged tympanic membrane, with atrophic or retracted areas, is a poor baroreceptor. It might therefore become subject to wider fluctuations of pressure, which would then further damage the atrophic part and continue the retraction process. ACKNOWLEDGEMENTS This study was financed in part by a grant from the Toronto Hong Kong Lions Club; and by the Department of Otolaryngology, the Hospital for Sick Children, Toronto, Canada. The authors are grateful to the Department of Statistics, University of Birmingham, UK, for statistical advice. Our thanks are also due to Dr. H. Koch, Department of Hyperbaric Medicine, Toronto General Hospital, for his suggestions and advice on some of the effects of pressure change on the ear.
REFERENCES 1. Tos M, Stangerup S E , Holm-Jensen S, Sprrensen CH. Spontaneous course of secretory otitis and changes in the eardrum. Arch Otolaryngol 1984; 110 281-9. 2. Lildholdt T, Courtois J, Kortholm B, Schou JW,Warrer H. The correlation between negative middle ear pressure and the corresponding conductive hearing loss in children. Sand Audio1 1979; 8: 117-20. 3. Hellstr6m S, Stenfon L-E. The pressure equilibrating function of the pars flaccida in middle ear mechanics. Acta Physiol Scand 1983; 118: 337-41.
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The middle ear as a baroreceptor
4. Magnuson B. On the origin of the high negative pressure in the closed middle ear space. Am J Otolaryngol 1981; 2: 1-12. 5. Sad6 J, Luntz M. Gaseous pathways in atelectatic ears. Ann Otol Rhino1 Laryngol 1989; 9 8 355-8. 6. Murphy D. Negative pressure in the middle ear by d i a r y propulsion of mucus through the eustachian tube. Laryngoscope 1979; 8 9 945-61. 7. Eden AR, Gannon PJ. Neural control of middle ear aeration. Arch Otolaryngol Head Neck Surg 1987; 113: 133-7. 8. Rockley TJ, Hawke WM. The glomus tympanicum: a middle ear chemoreceptor? J Otolaryngol 1990; 18: 7, 370-3. 9. Tjernstrom 0. Effects of middle ear pressure in the inner ear. Acta Otolaryngol (Stockh) 1977; 8 3 11-5. 10. Tonndorf J, Khanna SM. Tympanic membrane vibration of human cadavers ears studied by time-averaged holography. J Acoust Soc Am 1972; 5 2 1221-33. 11. Hamer M. Trains that go pop in the dark. New Scientist, 9th September 1989; 63-5. 12. Ramseen RT, Gibson WPR, Moffat DA. Anaesthesia of the tympanic membrane using iontophoresis. J Laryngol Otol 1976; 85: 779-84. 13. Cox DR, Oakes D. Analysis of survival data. London: Chapman and Hall, 1984. 14. Inglestedt S, Jonson B. Mechanisms of the gas exchange in the normal human middle ear. Acta Otolaryngol (Stockh) 1967; Suppl 224: 452-61. 15. Molvaer 01, Vallersnes FM, Kringlebotn M. The size of the middle ear and mastoid air cell. Acta Otolaryngol (Stockh) 1978; 8 5 24-32. 16. Hiittenbrink KB. The mechanics of the middle ear at static ear pressures. Acta Otolaryngol (Stockh) 1988; SUppl 451: 1-35. 17. Schrapnell HJ. On the form and structure of the membrane tympanii. London Medical Gazette 1832; 120: 120-4. 18. Stenfors L-E, Sal6n B, Winblad B. The role of the pars flaocida in the mechanics of the middle ear. Acta Otolaryngol (Stockh) 1979; 88: 395-400. 19. Aritomo H, Goode RL, Gonzalez J. The role of pars flaccida in human middle ear sound transmission. Otolaryngol Head Neck Surg 1988; 98: 310-4. 20. Lim DJ. Human tympanic membrane: An ultrastructural observation. Acta Otolaryngol (Stockh) 1970; 7 0 176-86. 21. Saunders RL, Weider D. Tympanic membrane sensation. Brain 1985; 108: 387-404. 22. Wilson JG. The nerves and nerve endings of the membrana tympanii of man. Am J Anat 1911; 11: 101-12. 23. Nagai T, Tono T. Encapsulated nerve corpuscles in the human tympanic membrane. Arch Otorhinolaryngol 1989; 246: 169-72. 24. Miller AJ. Deglutition. Physiol Rev 1982; 6 2 129-75. Manuscript received June 17, 1991; accepted February 13, 1992
Address for correspondence: W. M. Hawke, Ear Pathology Research Laboratory, CCRW 1.813, Toronto General Hospital, 100 Gollege St., Toronto, Ontario M5G 1L7, Canada
823
The Middle Ear as a Baroreceptor T. J. ROCKLEY‘ and W. M. HAWKE* From the ‘Department of Otolaryngology, Enrt Birmingham Hospital, Bordesley Green f i t , Birmingham, West MidlandF 3 9 5ST, UK and the 2Departments of Otolaryngology and Pathology, Unwersity of Toronto, Ontario, Canada
Acta Otolaryngol Downloaded from informahealthcare.com by University of Guelph on 09/13/12 For personal use only.
Rockley TJ, Hawke WM. The middle ear as a baroreceptor. Acta Otolaryngol (Stockh) 1992; 112 816-823. Underpressure in the middle ear is thought to be important in the pathogenesis of chronic otitis media with effusion and its sequelae, but the cause of the underpressure and the mechanisms responsible for regulation of the normal middle ear pressure are a matter of debate. Numerous studies have examined the effect of large pressure changes on the ear; however, the ear’s sensitivity to smaller pressure changes has received little attention. This study examines the sensitivity of the ear to atmosphericair pressure changes induced in the external ear canal. It is concluded that the normal ear is a very sensitive pressure receptor, and that the sensation is probably registered by stretch receptors in the tympanic membrane. Pathological changes in the tympanic membrane are associated with impaired baroreceptor function. The implications of these findings in the physiology of the ear and the regulation of middle ear presssure are discussed. Key words: middle ear pressure, tympanic membrane, stretch receptors, pressure receptors.
INTRODUCTION In the healthy ear, the gas pressure within the closed middle ear space is maintained close to atmospheric (1,2, 3). The origin of the abnormally low intratympanic pressures in middle ear disease states is at present controversial: it has been suggested (4) that the underpressure may arise suddenly from voluntary middle ear evacuation in patients with an abnormally patulous eustachian tube (the “sniffing theory”). The negative pressure may also arise more slowly from gas diffusion from the middle ear into the mucosa associated with deficient eustachian tube opening (S), or from a hydraulic effect of ciliary traction on middle ear mucus as it passes down the eustachian tube (6). The importance of understanding the physiology and pathophysiology of intratympanic pressure is evident, but at present the regulation of gas pressure in the normal ear is poorly understood. Pressure of gas within the middle ear is dependent on several factors; the composition of the gas, diffusion in and out of the mucosa, equilibration with the nasopharynx via opening of the eustachian tube, and active inflation or evacuation (e.g. by sniffing, noseblowing, or Valsalva’s manoeuvre). Chemoreceptive reflexes have been postulated (7) as a means of regulating middle ear pressure. The presence of chemoreceptor or glomus tissue in the middle ear mucosa has led to the suggestion that it may respond to gas composition changes in the middle ear, initiating “middle ear ventilation reflexes”, effected by the eustachian tube muscles. We have argued, however, that this is unlikely (8). Anatomically, glomus tissue has an angiochemoreceptor structure and is only inconstantly present in the middle ear mucosa. Very little attention has been paid to the phenomenon of baroreception in the middle ear and to the possible role pressure sensation might have in the regulation of middle ear pressure. This is in contrast to the considerable study that has been done (9) on the middle ear’s response to the large pressure variations that may occur in aeroplane fight and deep sea diving (causing such diseases as barotrauma, perilymph fistula, and alternobaric vertigo),
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Acta Otolaryngol (Stockh) I12
The middle ear ar a baroreceptor
and also to the tiny pressure vibrations that are sound waves (10). It is a matter of common experience that slight atmospheric pressure changes (for example those encountered when travelling in a train or car), or middle ear pressure changes (for example after blowing the nose), are registered in the ears causing a sensation of “fulness” and leading to a desire to “clear” the ears and re-equilibrate middle ear pressure. This sensation is an important consideration in the design of modern passenger transportation ( 1 1): air-pressure fluctuations in the carriages of high-speed trains must be kept to a level that is comfortable to passengers’ ears. This phenomenon is perhaps not surprising when one realises that the closed middle ear space is probably the only organ in the body that is structured as an air baroreceptor or pressure transducer. There is therefore the theoretical potential for baroreception in the ear, but this subject has thus far received little attention. The purpose of this study is to investigate the sensitivity of the ear to atmospheric pressure changes in both normal and pathological conditions; such information could provide some insight into the role of baroreception in the regulation of normal middle ear pressure, and how this system might fail in disease, resulting in middle ear underpressure.
MATERIAL AND METHOD Normal ears
Four experiments were performed on 28 volunteers (56 ears), aged between 19 and 50 years, with no history of chronic middle ear disease, and normal tympanic membranes at otomicroscopy. Each ear was tested separately using an impedance bridge apparatus (Peters AP67). This instrument, normally used for performing tympanometry, was modified by switching off the test tone, and after obtaining a comfortable airtight seal in the ear canal, the air pressure within the canal could be altered from -300 to +300mmH,O, the exact pressure being recorded on the instrument’s manometer. Adequacy of airtight seal was checked before and after each experiment by confirming that there was no variation in the manometer reading during induced static pressure changes. With this arrangement, several experiments were performed. To determine the subjective threshold of baroreception, the ear canal air pressure was increased or decreased from atmospheric at a constant rate of 50 mmH,O (50 decapascals) per 5 s. Subjects were asked to indicate the point at which they were first able to appreciate the change of pressure. The pressure level at which the subject responded on two out of three consecutive occasions was recorded as the threshold. Positive and negative pressure were tested separately. Adaptation of the pressure sensution. A positive pressure of 50 mmH,O above threshold was introduced into the ear canal and maintained for 3min. The subject was asked to indicate during that time period the point at which he or she was no longer aware of the sensation of pressure, thus providing an indication of physiological adaptation of the sensation. Specifirfty of the response. To determine whether the ear could distinguish between positive and negative pressure as a sensation, subjects were presented five times with pressures in the ear canal at 50mmH,O above threshold, either positive or negative, and asked to say whether they thought the pressure was positive or negative. Effect of iontophoresis. Subjective thresholds of baroreception in five subjects were retested after anaesthetising the tympanic membrane with a 2% lignocaine/l:2OOO adrenaline solution, using the technique of iontophoresis (12).
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Acta Otolaryngol (Stockh) 112
Abnormal ears Thresholds to positive pressure change induced in the ear canal as described above were determined for 39 ears with otoscopically abnormal tympanic membranes (in 28 adult patients) without middle ear effusion or otorrhoea, attending an otologcal outpatient clinic. The abnormalities, which are regarded as long-term sequelae of otitis media with effusion (1) (listed below), were categorised as being either “minor” or “major”. To avoid possible tympanic membrane perforation in this group, some of whom had very atrophic membranes, pressure changes were limited to those encountered in routine tympanometry, i.e. a maximum of +200 mmH,O. Minor abnormalities (26 ears). Isolated patch of tympanosclerosis and atrophic segment of pars tensa were seen as well as retraction of the pars flaccida with adhesion to the neck of malleus; but without erosion of the notch of Rivinus, and with the depths of the retraction being fully visible otoscopically. Moreover, retraction of the posterior segment of the pars tensa, with adhesion to the incudostapedial joint, but with the depths of the retraction being fully visible otoscopically. Major abnormaliries (13 ears). Tympanosclerosisor atrophy affecting more than half of the pars tensa was noted as well as deep retraction of the pars flaccida, the full extent of the retraction not apparent on otoscopy, with or without erosion of the notch of Rivinus (but without cholesteatoma formation). Deep retraction of the posterior segment of the pars tensa into the sinus facialis or sinus tympani was also seen and a combination of the above abnormalities.
RESULTS Buroreception thresholds (see Fig. 1). This graph shows the range of subjective thresholds to pressure changes in the 56 normal ears tested. It was noted during testing that once an individual became familiar with the sensation, responses to positive pressure became very
HEOATWE PRESSURE
-lo
POMlVE PRESSURE mnlH*O
Fig. I. Thresholds of subjective sensitivity to pressure change in the ear canal, as found in 56 normal ears.
The middle ear as a baroreceptor 819
Acta Otolaryngol (Stockh) 112
consistent for that individual, usually within 25 mmH,O of each other on repeat testing. Responses to negative pressure were more variable and less precise than for positive pressure. The responses to positive pressure in the ear canal are, however, more relevant to the clinical situation, as the tympanic membrane is displaced medially, simulating retraction. It may be seen that although there is variation between individuals in the subjective thresholds, the majority of people responded to pressures of less than 100 mmH,O. Adaptation (see Fig. 2). In all but one of the ears tested, the sensation of “fulness” in the ear was lost during the 3 min of the test despite the pressure in the ear canal being sustained, indicating that sensory adaptation takes place.
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+
Fig. 2. Adaptation of the pressure sensation. This graph shows the number of individuals who remained subjectively aware of a sustained positive pressure during a 3-minute test period (25 normal subjects, ears tested separately).
Minutes NUYEER
0
25
50
75
100
125
150
175
200
-200
PoSmvE PRESSURE rnrnH 0
Fig. 3. Threshold of subjective sensitivity to pressure change in the ear canal, as found in 39 abnormal ears.
820 T. J . Rockley and W . M . Hanke
Acta Otolaryngol (Stockh) 112
Table I. Baroreception thresholds before and a f e r iontophoresis
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Subject 1 Subject 2 Subject 3 Subject 4 Subject 5
Thresholds (mmH,O)
Thresholds after iontophoresis (mmH20)
- 100
None obtained from -300 to f 3 0 0 None obtained from -300 to +300 -200 +200 -225 + 300 -200None obtained to +300
- 150
+50 t75
- 100 -75
+ 130
- 125
i75
i-60
Specificity of discrimination between positiw and negatiue pressure. None of the subjects tested were able to distinguish subjectively between positive and negative pressure in the ear canal. The effect of iontophoresis (see Table I). In the 5 subjects whose thresholds to positive and negative pressure were retested after lignocaine iontophoresis, the ear became less sensitive to pressure change as a result of the local anaesthesia, as seen in Table I. Baroreception threshold in diseased ears (see Fig. 3 ) . Subjects with abnormalities of the tympanic membrane had impaired sensation to pressure change, as may be seen if Fig. 3 is compared with the distribution of baroreception thresholds for positive pressure in normal ears (Fig. 1). Statistical comparison of the results between the two groups (Mantel-Haenzel test) shows that this difference is significant: Chi-squared = 16.4, 1 degree of freedom; p < 0.001 (13). In general, more Severe tympanic membrane abnormalities were associated with less sensitive ears: for 10 ears tested, no threshold could be obtained within the test range of 0-200 mmH,O.
DISCUSSION The ear as a baroreceptor. It would appear from these results that the healthy ear is a Sensitive baroreceptor to air pressure changes induced in the ear canal, the threshold of sensitivity (for positive pressure) in most of the subjects tested being within the “normal range” of middle ear pressure accepted for tympanometry readings. Inducing a negative pressure in the ear canal gave more variable responses, possibly because it caused some venous filling and hence a volume change in the ear canal skin and pars flaccida, mitigating tympanic membrane displacement. To give some perspective on the ear’s sensitivity, Fig. 4
1.-12
Fig. 4. Displacement of the tympanic membrane in response to induced air-pressure changes. AP = Static air-pressure in the external ear canal AVtm = induced volume change in the position of the tympanic membrane. (Redrawn from (14) with permission of the Editor of Acta Otolaryngologica).
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Acta Otolaryngol (Stockh) 112
The middle ear as a baroreceptor
shows the volume displacement of the tympanic membrane in response to induced pressure changes in the ear canal (14). As already noted, most subjects were aware of pressure changes of less than 100 mmH,O, and this corresponds to a volume displacement of the TM of less than 15 pl. Considering that on average the volume of the middle ear and mastoid air cells, is 6 OW p1 ( 15), it can be seen that the ear thus may be sensitive to changes of a fraction of one percent of that volume. It seems likely from experiment 2, however, that this sensitivity is only for rapidly occurring pressure changes, because sensory adaptation takes place; and therefore slowly occurring changes in middle ear pressure relative to the atmosphere are probably not registered by this baroreceptor mechanism. This study is of practical relevance when one considers that passenger ear discomfort is an important factor in the design of modem railways, including the new Channel Tunnel rail link between England and France (1 1). High-speed trains cause air-pressure changes when they enter tunnels, and the resulting ear sensation is distressing to some passengers. The anatomical site of baroreception. When the air pressure in the ear canal is altered, movement occurs in the tympanic membrane, ossicular chain, tympanic muscles, and labyrinthine window membranes ( 16). The baroreception sensation could conceivably be registered by distortion of the malleoincudal joint or tensor tympani tendon, as both of these have been shown to play an important role in the mechanics of the middle ear, limiting hydraulic damage to the labyrinth when the malleus is displaced. The lack of discrimination noted in our study between positive and negative pressure, and the diminished sensitivity after iontophoresis, suggest that the tympanic membrane itself is the origin of the barorecep tion sensation. This idea, that the tympanic membrane is somehow involved with middle ear pressure regulation, is not new. Schrapnell, over 150 years ago, in his classic description of the tympanic membrane (17) suggested different roles for the two parts: the pars tensa was relatively stiff and functioned primarily for sound conduction, while the pars flaccida was displaced more easily and accommodated pressure fluctuations. Stenfors et al. in 1979 (18) supported this concept in their experiments on pressure-induced displacement of the pars flaccida of rats, but later (3), realising that the volumes of gas that might be accommodated by this mechanism were relatively insignificant, proposed that the pars flaccida was actually a sensor mechanism for pressure fluctuations in the middle ear. This is an attractive idea, particularly since the pars flaccida does not seem to have the demonstrable role in sound transmission (19). The pars flaccida contains elastin fibres while the pars tensa does not (20); this arrangement echoes the structure of the arterial baroreceptor in the carotid sinus, whose wall is more elastic and distensible than the adjacent carotid artery. At present, it is not known whether stretch receptors exist within the tympanic membrane. Saunders & Weider (21), in their study entitled “Tympanic membrane sensation”, described it as apparently exclusively a nociceptive system. It may be that the specialised nerve endings in the pars tensa described originally by Wilson (22) in 1911 as “modified pacinian corpuscles” and rediscovered recently by Nagai & Tono (23) might be sensitive to tympanic membrane displacement (as suggested by Nagai & Tono), but this remains to be elucidated. We are currently undertaking studies on whole-mount cadaver tympanic membrane preparations to look at the distribution of these encapsulated endings in the pars tensa and flaccida. Baroreception in middle ear physiology and pathophysiology. As a result of our experiments, we would suggest the following role for baroreception in the non-auditory physiology of the ear. It seems to register short-term changes in middle ear pressure relative to atmospheric pressure in the conscious subject, the sort of pressure changes that might be caused by activity, e.g. sneezing, valsalva, sniffing or nose-blowing; leading to voluntary tubal opening and pressure equilibration by swallowing or yawning. It is interesting to note that the volume of air that may pass up the eustachian tube to the ear by tubal opening during a swallow is
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822 T. J . Rockley and W. M. Hawke
Ac- ~ o ~ g(Stockh) o l 112
approximately I5 PI ( 14); the same volume change that would cause a feeling of “fulness in the ear” for most subjects in our study. This protective mechanism would prevent damage to the tympanic membrane from excessive mechanical distortion, and also allow the sound conduction mechanism of the ear to function optimally. Slower middle ear pressure changes, for example from diffusion of gas into and out of the middle ear mucosa, are probably not consciously registered; but these changes are equilibrated easily by the frequent swallowing actions that occur normally throughout the day (average 10 per hour) in response to saliva in the pharynx (24), and which open the eustachian tube. Finally, we may speculate on the role of the middle ear baroreceptor mechanism in disease states characterised by intratympanic underpressure. Studies performed by Magnuson and his coworkers (4) have demonstrated that negative middle ear pressure may be induced suddenly by sniffing in certain individuals who suffer from the symptoms of intermittent patulous eustachian tube. This voluntary evacuation of the ear causes “locking” of the tube, thereby eliminating troublesome autophony. If repeated over a long time, middle ear atelectasis and cholesteatoma may ensure. From our studies, it would seem possible that the initial discomfort experienced by such individuals resulting from sudden evacuation of the ear would soon diminish as adaptation takes place, and retraction pocket formation would be accompanied by a further impairment of pressure application, allowing more damage to occur. Negative pressure may, however, develop in the middle ear more slowly. Sad6 & Luntz ( 5 ) showed gradual retraction of the tympanic membrane to its original position over 60min following air politzerisation of an atelectatic ear, due to diffusion of gas into the middle ear mucosa. In an experiment on cats, Murphy (6) demonstrated that mucus introduced into the middle ear was slowly cleared by ciliary action down the eustachian tube, and this was associated with the development of negative pressure in the ear caused by a hydraulic effect of the moving mucus column. We would suggest that slowly developing underpressures such as these would not cause symptoms in the ear, again because of adaptation of the sensation of pressure change, and therefore voluntary attempts to re-equilibrate the ears would not be made. Impaired baroreceptor function may play a part in the pathogenesis of retraction pockets of the tympanic membrane: it appears from our study that a damaged tympanic membrane, with atrophic or retracted areas, is a poor baroreceptor. It might therefore become subject to wider fluctuations of pressure, which would then further damage the atrophic part and continue the retraction process. ACKNOWLEDGEMENTS This study was financed in part by a grant from the Toronto Hong Kong Lions Club; and by the Department of Otolaryngology, the Hospital for Sick Children, Toronto, Canada. The authors are grateful to the Department of Statistics, University of Birmingham, UK, for statistical advice. Our thanks are also due to Dr. H. Koch, Department of Hyperbaric Medicine, Toronto General Hospital, for his suggestions and advice on some of the effects of pressure change on the ear.
REFERENCES 1. Tos M, Stangerup S E , Holm-Jensen S, Sprrensen CH. Spontaneous course of secretory otitis and changes in the eardrum. Arch Otolaryngol 1984; 110 281-9. 2. Lildholdt T, Courtois J, Kortholm B, Schou JW,Warrer H. The correlation between negative middle ear pressure and the corresponding conductive hearing loss in children. Sand Audio1 1979; 8: 117-20. 3. Hellstr6m S, Stenfon L-E. The pressure equilibrating function of the pars flaccida in middle ear mechanics. Acta Physiol Scand 1983; 118: 337-41.
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4. Magnuson B. On the origin of the high negative pressure in the closed middle ear space. Am J Otolaryngol 1981; 2: 1-12. 5. Sad6 J, Luntz M. Gaseous pathways in atelectatic ears. Ann Otol Rhino1 Laryngol 1989; 9 8 355-8. 6. Murphy D. Negative pressure in the middle ear by d i a r y propulsion of mucus through the eustachian tube. Laryngoscope 1979; 8 9 945-61. 7. Eden AR, Gannon PJ. Neural control of middle ear aeration. Arch Otolaryngol Head Neck Surg 1987; 113: 133-7. 8. Rockley TJ, Hawke WM. The glomus tympanicum: a middle ear chemoreceptor? J Otolaryngol 1990; 18: 7, 370-3. 9. Tjernstrom 0. Effects of middle ear pressure in the inner ear. Acta Otolaryngol (Stockh) 1977; 8 3 11-5. 10. Tonndorf J, Khanna SM. Tympanic membrane vibration of human cadavers ears studied by time-averaged holography. J Acoust Soc Am 1972; 5 2 1221-33. 11. Hamer M. Trains that go pop in the dark. New Scientist, 9th September 1989; 63-5. 12. Ramseen RT, Gibson WPR, Moffat DA. Anaesthesia of the tympanic membrane using iontophoresis. J Laryngol Otol 1976; 85: 779-84. 13. Cox DR, Oakes D. Analysis of survival data. London: Chapman and Hall, 1984. 14. Inglestedt S, Jonson B. Mechanisms of the gas exchange in the normal human middle ear. Acta Otolaryngol (Stockh) 1967; Suppl 224: 452-61. 15. Molvaer 01, Vallersnes FM, Kringlebotn M. The size of the middle ear and mastoid air cell. Acta Otolaryngol (Stockh) 1978; 8 5 24-32. 16. Hiittenbrink KB. The mechanics of the middle ear at static ear pressures. Acta Otolaryngol (Stockh) 1988; SUppl 451: 1-35. 17. Schrapnell HJ. On the form and structure of the membrane tympanii. London Medical Gazette 1832; 120: 120-4. 18. Stenfors L-E, Sal6n B, Winblad B. The role of the pars flaocida in the mechanics of the middle ear. Acta Otolaryngol (Stockh) 1979; 88: 395-400. 19. Aritomo H, Goode RL, Gonzalez J. The role of pars flaccida in human middle ear sound transmission. Otolaryngol Head Neck Surg 1988; 98: 310-4. 20. Lim DJ. Human tympanic membrane: An ultrastructural observation. Acta Otolaryngol (Stockh) 1970; 7 0 176-86. 21. Saunders RL, Weider D. Tympanic membrane sensation. Brain 1985; 108: 387-404. 22. Wilson JG. The nerves and nerve endings of the membrana tympanii of man. Am J Anat 1911; 11: 101-12. 23. Nagai T, Tono T. Encapsulated nerve corpuscles in the human tympanic membrane. Arch Otorhinolaryngol 1989; 246: 169-72. 24. Miller AJ. Deglutition. Physiol Rev 1982; 6 2 129-75. Manuscript received June 17, 1991; accepted February 13, 1992
Address for correspondence: W. M. Hawke, Ear Pathology Research Laboratory, CCRW 1.813, Toronto General Hospital, 100 Gollege St., Toronto, Ontario M5G 1L7, Canada
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