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Figure 1.
Measured area. The outline of the mastoid air cell system was traced on an x-ray film, and its area was measured using an image analysis program (National Institutes of Health, Rockville, Md).

Measured area. The outline of the mastoid air cell system was traced on an x-ray film, and its area was measured using an image analysis program (National Institutes of Health, Rockville, Md).

Figure 2.
Response of middle ear pressure (MEP) to the respiratory mode. Hyper indicates hyperventilation; Hypo, hypoventilation; a, at the beginning of the examination; b, at the end of the initial hyperventilation; c, at the end of the hypoventilation; d, at the end of the final hyperventilation; and daPa, decapascals. Hyperventilation and hypoventilation are given with duration in each respiratory mode (minutes). Hyperventilation and hypoventilation are given with duration in each respiratory mode (minutes). Results are shown from subject 1 of the good-response group (A), subject 11 of the good-response group (B), and subject 13 of the poor-response group (C). In subject 11, swallowing was observed during the hypoventilation, and a rapid increase of MEP that was thought to be caused by the gas exchange via the eustachian tube was noted (arrow). Swallowing and coughing occurred repeatedly in subject 13 during the initial hyperventilation (arrow), and MEP showed little change after that.

Response of middle ear pressure (MEP) to the respiratory mode. Hyper indicates hyperventilation; Hypo, hypoventilation; a, at the beginning of the examination; b, at the end of the initial hyperventilation; c, at the end of the hypoventilation; d, at the end of the final hyperventilation; and daPa, decapascals. Hyperventilation and hypoventilation are given with duration in each respiratory mode (minutes). Hyperventilation and hypoventilation are given with duration in each respiratory mode (minutes). Results are shown from subject 1 of the good-response group (A), subject 11 of the good-response group (B), and subject 13 of the poor-response group (C). In subject 11, swallowing was observed during the hypoventilation, and a rapid increase of MEP that was thought to be caused by the gas exchange via the eustachian tube was noted (arrow). Swallowing and coughing occurred repeatedly in subject 13 during the initial hyperventilation (arrow), and MEP showed little change after that.

Table 1. 
PvCO2, PVO2, and Middle Ear Pressure in Each Respiratory Mode*
PvCO2, PVO2, and Middle Ear Pressure in Each Respiratory Mode*
Table 2. 
Degree of Change of Middle Ear Pressure and PvCO2 in Good-Response Group
Degree of Change of Middle Ear Pressure and PvCO2 in Good-Response Group
1.
Ikarashi  F The effect of respiratory mode on human middle ear pressure. Auris Nasus Larynx. 1998;25349- 354Article
2.
Rundcrantz  H Posture and eustachian tube function. Acta Otolaryngol (Stockh). 1969;68279- 292Article
3.
Takahashi  HHonjo  INaito  Y  et al.  Gas exchange function through the mastoid mucosa in ears after surgery. Laryngoscope. 1997;1071117- 1121Article
4.
Ars  BWuyts  FVan de Heyning  PMiled  IBogers  JVan Marck  E Histomorphometric study of the normal middle ear mucosa: preliminary results supporting the gas-exchange function in the postero-superior part of the middle ear cleft. Acta Otolaryngol (Stockh). 1997;117704- 707Article
5.
Flisberg  KZsigmond  M The size of the mastoid air cell system: planimetry: direct volume determination. Acta Otolaryngol (Stockh). 1965;6023- 29Article
6.
Ingelstedt  S Chronic adhesive otitis: analysis of some predisposing factors. Acta Otolaryngol (Stockh). 1964;18819- 28Article
7.
Flisberg  K The effects of vacuum on the tympanic cavity. Otolaryngol Clin North Am. 1970;33- 13
8.
Elner  Å Indirect determination of gas absorption from the middle ear. Acta Otolaryngol (Stockh). 1972;74191- 196Article
9.
Elner  Å Normal gas exchange in the human middle ear. Ann Otol Rhinol Laryngol. 1976;85(suppl 25)161- 164
10.
Buckingham  RAStuart  DRGeick  MRGirgis  SJMcGee  TJ Experimental evidence against middle ear oxygen absorption. Laryngoscope. 1985;95437- 442
11.
Mover-Lev  HLevy  DLuntz  MHarell  MAr  ASadé  J Dependence of middle ear gas composition on pulmonary ventilation. Ann Otol Rhinol Laryngol. 1997;106314- 319
12.
Hergils  LMagnuson  B Regulation of negative middle ear pressure without tubal opening. Arch Otolaryngol Head Neck Surg. 1988;1141442- 1444Article
13.
Hergils  LMagnuson  B Morning pressure in the middle ear. Arch Otolaryngol Head Neck Surg. 1985;11186- 89Article
14.
Shinkawa  HOkitsu  TYusa  TYamamuro  MKaneko  Y Positive intratympanic pressure in the morning and its etiology. Acta Otolaryngol (Stockh). 1987;435107- 111Article
15.
Doyle  WJSeroky  JT Middle ear gas exchange in rhesus monkeys. Ann Otol Rhinol Laryngol. 1994;103636- 645
16.
Sadé  JLuntz  MLevy  D Middle ear gas composition and middle ear aeration. Ann Otol Rhinol Laryngol. 1995;104369- 373
17.
Luntz  MLevi  DSadé  JHerman  M Relationship between the gas composition of the middle ear and the venous blood at steady state. Laryngoscope. 1995;105510- 512Article
18.
Ikarashi  FNakano  YOkura  T Pneumatization of the tympanic bulla after blockage of the ventilation route through the eustachian tube in the pig. Ann Otol Rhinol Laryngol. 1996;105784- 790
19.
Tideholm  BCarlborg  BJönsson  SBylander-Groth  A Continuous long-term measurements of the middle ear pressure in subjects without a history of ear disease. Acta Otolaryngol (Stockh). 1998;118369- 374Article
20.
Yamamoto  Y Gas exchange function through the middle ear mucosa in piglets: comparative study of normal and inflamed ears. Acta Otolaryngol (Stockh). 1999;11972- 77Article
Original Article
September 1999

Carbon Dioxide Exchange via the Mucosa in Healthy Middle Ear

Author Affiliations

From the Departments of Otolaryngology, The Nippon Dental University School of Dentistry at Niigata (Dr Ikarashi), and the Niigata University School of Medicine (Drs Takahashi and Yamamoto), Niigata, Japan.

Arch Otolaryngol Head Neck Surg. 1999;125(9):975-978. doi:10.1001/archotol.125.9.975
Abstract

Background  Recent studies have shown that gas exchange via the middle ear mucosa, which is performed between the middle ear cleft and capillaries in the submucosal connective tissue, has an essential role in ventilation and pressure regulation in the middle ear cleft. We speculated that gas exchange via the mucosa is induced by the gas diffusion caused by the partial pressure gradient of gas between the middle ear cleft and submucosal capillaries.

Objective  To evaluate the capacity of the gas exchange via the mucosa in the healthy middle ear of humans by examining the effect of the respiratory mode on middle ear pressure.

Subjects and Methods  We selected 13 volunteers ranging in age from 25 to 44 years with healthy ear drums and type A tympanograms. Middle ear pressure was measured in 1 ear of each subject every 2 minutes using tympanometry while the respiratory mode was altered, with the subject in the supine position.

Results  The partial pressure of carbon dioxide in the venous blood (PvCO2) and middle ear pressure were decreased by hyperventilation and increased by hypoventilation. The partial pressure of oxygen in the venous blood showed little change.

Conclusions  Carbon dioxide diffused into the blood from the middle ear cleft in accord with the partial pressure gradient when the PvCO2 was reduced by hyperventilation, resulting in a decrease of middle ear pressure, whereas CO2 diffused into the middle ear cleft when the PvCO2 was elevated by hypoventilation, resulting in an increase of middle ear pressure. These findings suggest that a bidirectional CO2 exchange via the middle ear mucosa functions in the normal human middle ear.

CONCERNING the mechanism of gas exchange in the middle ear cleft, gas exchange via the middle ear mucosa in addition to that via the eustachian tube has been investigated, and the existence of this gas exchange has been confirmed clinically and experimentally. In a preliminary study, the possibility that gas exchange via the middle ear mucosa functions because human middle ear pressure was decreased by hyperventilation and increased by hypoventilation was observed.1 In our present study, a more precise examination was performed to clarify these findings.

SUBJECTS AND METHODS

We selected 13 volunteers (12 men and 1 woman) ranging in age from 25 to 44 years with healthy ear drums, type A tympanograms, and no history of middle ear diseases or middle ear surgery. We carefully enlisted the volunteers who met the study criteria and obtained informed consent, and 13 of them remained eligible. We postulated that if gas exchange occurs via the mucosa, the partial pressures of blood gases might change according to the alteration of the respiratory mode, resulting in a change in middle ear pressure. We performed this study to test this hypothesis.

Tympanometry was performed in 1 ear of each subject at every 2 minutes while the respiratory mode was altered from initial hyperventilation to hypoventilation, followed by final hyperventilation, with the subject in the supine position to avoid as much as possible the effect of gas exchange via the eustachian tube. This was because the capacity of the ventilation via the eustachian tube is diminished in the supine position compared with the sitting position.2 Pressure in the external auditory canal corresponding to the peak of the tympanogram (Impedance Audiometer RS-20; RION, Tokyo, Japan) was taken as the middle ear pressure. Hyperventilation was achieved by having the subject breathe as quickly and deeply as possible, whereas hypoventilation was achieved by breathing as slowly and lightly as possible. Each respiratory mode was maintained until an apparent change of middle ear pressure was induced. All subjects were instructed to swallow as little as possible. In all subjects, a blood sample was withdrawn from the median cubital vein for blood gas analysis at the beginning of the examination, at the time of change of the respiratory mode, and at the end of the examination. An ear x-ray film (Schüller view) was obtained, and the entire area of the mastoid air cell system was calculated using an image analysis computer software program (National Institutes of Health, Rockville, Md) (Figure 1).

We obtained the approval of the ethics committee of The Nippon Dental University School of Dentistry at Niigata, Niigata, Japan, where this study was performed.

RESULTS

The partial pressure of carbon dioxide (CO2) in the venous blood (PvCO2) and middle ear pressure were decreased significantly at the end of the initial hyperventilation compared with that at the beginning of the examination, increased at the end of the hypoventilation compared with that at the end of the initial hyperventilation, and decreased at the end of the final hyperventilation compared with that at the end of the hypoventilation (Table 1) (paired t test, P<.001). The partial pressure of oxygen in the venous blood (PvO2) showed little change related to the respiratory condition.

In 11 of the 13 subjects, the middle ear pressure was decreased slowly by hyperventilation and increased slowly by hypoventilation (good-response group, subjects 1-11; Figure 2, A); in 4 subjects in the good-response group, a rapid change of the middle ear pressure accompanied by swallowing was observed once (subjects 8-11; Figure 2, B). In the remaining 2 subjects, no apparent change of the middle ear pressure related to the respiratory condition was observed (poor-response group, subjects 12 and 13; Figure 2, C).

The mastoid air cell system in the normal ears might play an important role in gas exchange via the mucosa,3,4 and its volume is reported to be directly proportional to the area that was measured using planimetry (on x-ray film).5 Therefore, the entire area of the mastoid air cell system of our good-response group was measured from x-ray films, and the degrees of the change of the middle ear pressure per unit of duration (10 minutes) and per unit of change in PvCO2 (10 mm Hg) were calculated. Although the development of the mastoid air cell system was satisfactory in all ears, the degree of the change of middle ear pressure varied in each respiratory mode within the same subjects as well as among the subjects (Table 2). In the poor-response group, swallowing and coughing occurred repeatedly during the initial hyperventilation, and a stable respiratory condition could not be maintained.

COMMENT

It has generally been accepted that gas in the middle ear cleft is continuously absorbed into the surrounding tissue, with air being supplied into the middle ear through the eustachian tube, and that the middle ear pressure decreases when the eustachian tube is obstructed.69 However, in recent research, it is becoming evident that gas exchange via the middle ear mucosa, which is performed between the middle ear cleft and capillaries in the submucosal connective tissue, plays an important role in the ventilation and pressure regulation of the middle ear cleft. It was suggested that gas exchange via the mucosa is induced by the gas diffusion caused by the partial pressure gradient of gas between the middle ear cleft and submucosal capillaries.1020 A correlation between PvCO2 and middle ear pressure has been documented in animal experiments and clinical studies,1017,19,20 and we observed the possibility that gas exchange via the middle ear mucosa functions, since human middle ear pressure was decreased by hyperventilation and increased by hypoventilation.1

In our study, PvCO2 and middle ear pressure were decreased by hyperventilation, whereas they were increased by hypoventilation. Although there are no direct measures of CO2 in the middle ear cleft, we suspect that CO2, which has a rapid diffusion rate,15 diffuses quickly into the blood from the middle ear cleft according to the partial pressure gradient when PvCO2 is reduced by hyperventilation, resulting in a decrease of the middle ear pressure. On the other hand, CO2 diffuses into the middle ear cleft when PvCO2 is elevated by hypoventilation, resulting in an increase of the middle ear pressure. Our present findings suggest that a bidirectional gas exchange between the middle ear cleft and capillaries in the submucosal connective tissue occurs in the human middle ear. The PvO2 showed little change. During breathing of air in the normal atmosphere, the partial pressure of oxygen in the blood may not readily change with a simple alteration of spontaneous respiration.

The degrees of the change of the middle ear pressure per unit of duration and per unit of change of PvCO2 varied within subjects as well as among the subjects. We speculate that the capacity of gas exchange via the mucosa is not constant but rather is changed by surrounding circumstances, such as the number of submucosal capillaries, the volume of blood flow, and the condition of the middle ear mucosa. The effect of the partial pressure changes of oxygen and nitrogen cannot be denied, as well. In our poor-response group, swallowing and coughing occurred repeatedly. By these actions, gas exchange via the eustachian tube was repeated, which inhibited the change of middle ear pressure induced by the alteration of the respiratory mode.

Gas exchange via the mucosa can be accelerated when submucosal capillaries dilate and blood flow increases due to the middle ear inflammation, whereas it can be diminished when the mucosa thickens and submucosal connective tissue proliferates due to prolonged inflammation. We next hope to elucidate the relationship between middle ear inflammation and gas exchange via the mucosa.

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Article Information

Accepted for publication May 13, 1999.

Reprints: Fumio Ikarashi, MD, Department of Otolaryngology, The Nippon Dental University School of Dentistry at Niigata, Hamauracho 1-8, Niigata 951-8580, Japan (e-mail: jibika@ngt.ndu.ac.jp).

References
1.
Ikarashi  F The effect of respiratory mode on human middle ear pressure. Auris Nasus Larynx. 1998;25349- 354Article
2.
Rundcrantz  H Posture and eustachian tube function. Acta Otolaryngol (Stockh). 1969;68279- 292Article
3.
Takahashi  HHonjo  INaito  Y  et al.  Gas exchange function through the mastoid mucosa in ears after surgery. Laryngoscope. 1997;1071117- 1121Article
4.
Ars  BWuyts  FVan de Heyning  PMiled  IBogers  JVan Marck  E Histomorphometric study of the normal middle ear mucosa: preliminary results supporting the gas-exchange function in the postero-superior part of the middle ear cleft. Acta Otolaryngol (Stockh). 1997;117704- 707Article
5.
Flisberg  KZsigmond  M The size of the mastoid air cell system: planimetry: direct volume determination. Acta Otolaryngol (Stockh). 1965;6023- 29Article
6.
Ingelstedt  S Chronic adhesive otitis: analysis of some predisposing factors. Acta Otolaryngol (Stockh). 1964;18819- 28Article
7.
Flisberg  K The effects of vacuum on the tympanic cavity. Otolaryngol Clin North Am. 1970;33- 13
8.
Elner  Å Indirect determination of gas absorption from the middle ear. Acta Otolaryngol (Stockh). 1972;74191- 196Article
9.
Elner  Å Normal gas exchange in the human middle ear. Ann Otol Rhinol Laryngol. 1976;85(suppl 25)161- 164
10.
Buckingham  RAStuart  DRGeick  MRGirgis  SJMcGee  TJ Experimental evidence against middle ear oxygen absorption. Laryngoscope. 1985;95437- 442
11.
Mover-Lev  HLevy  DLuntz  MHarell  MAr  ASadé  J Dependence of middle ear gas composition on pulmonary ventilation. Ann Otol Rhinol Laryngol. 1997;106314- 319
12.
Hergils  LMagnuson  B Regulation of negative middle ear pressure without tubal opening. Arch Otolaryngol Head Neck Surg. 1988;1141442- 1444Article
13.
Hergils  LMagnuson  B Morning pressure in the middle ear. Arch Otolaryngol Head Neck Surg. 1985;11186- 89Article
14.
Shinkawa  HOkitsu  TYusa  TYamamuro  MKaneko  Y Positive intratympanic pressure in the morning and its etiology. Acta Otolaryngol (Stockh). 1987;435107- 111Article
15.
Doyle  WJSeroky  JT Middle ear gas exchange in rhesus monkeys. Ann Otol Rhinol Laryngol. 1994;103636- 645
16.
Sadé  JLuntz  MLevy  D Middle ear gas composition and middle ear aeration. Ann Otol Rhinol Laryngol. 1995;104369- 373
17.
Luntz  MLevi  DSadé  JHerman  M Relationship between the gas composition of the middle ear and the venous blood at steady state. Laryngoscope. 1995;105510- 512Article
18.
Ikarashi  FNakano  YOkura  T Pneumatization of the tympanic bulla after blockage of the ventilation route through the eustachian tube in the pig. Ann Otol Rhinol Laryngol. 1996;105784- 790
19.
Tideholm  BCarlborg  BJönsson  SBylander-Groth  A Continuous long-term measurements of the middle ear pressure in subjects without a history of ear disease. Acta Otolaryngol (Stockh). 1998;118369- 374Article
20.
Yamamoto  Y Gas exchange function through the middle ear mucosa in piglets: comparative study of normal and inflamed ears. Acta Otolaryngol (Stockh). 1999;11972- 77Article
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