Galioto GB (ed): Tonsils: A Clinically Oriented Update. Adv Otorhinolaryngol. Basel, Karger, 1992, vol 47, pp 290-296
Adenoids and Otitis media with Effusion in Children Tetsuo Watanabe, Tatsuya Fujiyoshi, Kazuhiro Tomonaga, GoroMogi Department of Otolaryngology, Oita Medical University, Oita, Japan
Adenoids have long been recognized as an important factor in the pathogenesis of otitis media with effusion (OME). There have been some reports that adenoidectomy was a useful procedure for correction of medically resistant OME. However, there is still much debate about whether the adenoids play an important role in the etiology of OME, and there have been no detailed investigations of the adenoids of patients both with OME and without OME. The purpose of this study is to compare adenoids both with OME and without OME, and to determine whether adenoids may be a cause of OME.
Materials and Methods Over the past 10 years, 171 patients have undergone adenoidectomy under general anesthesia at the Oita Medical University (Japan). Their ages ranged from 0 to 35 years (mean age, 6 years). One hundred and sixty-five of the 171 patients (96%) were from 2 to 15 years old. One hundred and six of those 171 patients had OME; the other 65 did not. In this study, we compared adenoids both with OME and without OME, clinically, histologically, and bacteriologically.
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Clinical Study In the clinical study, we selected 88 patients from 5 to 7 years of age. Fifty-nine of those 88 patients had OME; the other 29 did not have OME. We evaluated the size of adenoids from two perspectives: macroscopic size and relative size. The macroscopic size of the adenoid was examined using an indirect mirror or flexible fiberscope. They were graded from 0 to IV, defined as follows [1]: grade 0, no obvious lymphoid tissue on the posterior wall, including the roof of the nasopharynx, or no enlargement below the level of the superior margin of the choanae; grade I, enlarge-
Adenoids and OME
291
ment reaching the superior margin of the choanae; grade II, enlargement covering one third to one half of the choanae; grade III, enlargement covering one half to two thirds of the choanae; and grade IV, enlargement covering the choanae by more than two thirds. The relative size of adenoids was measured by lateral skull radiography as an adenoidalnasopharyngeal ratio (AIN ratio) obtained by dividing the adenoidal thickness by the nasopharyngeal distance [2]. Also, we examined the incidence of patients who had sinusitis and nasal allergy. Histological Study In the histological study, we selected the same patients as in the clinical study mentioned above for light microscopy. Patients whose ages ranged from 2 to 15 years were selected for scanning electron microscopy (SEM). For light microscopy, adenoids from patients were examined by the standard method: embedded in paraffin and stained with hematoxylin and eosin. The specimens were also placed in Karnovsky's fixative (2.5% glutaraldehyde and 2 % paraformaldehyde in 0.2 M cacodylate buffer pH 7.4) for 2-3 h. Standard methods were used for SEM. Also for SEM, the prefixed tissue specimens were postfixed in buffered 2 %osmium tetraoxide for 2 h ,dehydrated through graded concentrations of ethanol, and dried with t-butyl alcohol. The specimens were coated with gold and examined with a scanning electron microscope (S-800; Hitachi, Tokyo, Japan). Light microscopy was centered on the development of the germinal centers and the reticular formation of the epithelium. To evaluate the development of the germinal centers, we measured the area of the germinal center with a Nexus 6800 image processor (Kashiwagi Research Co. , Tokyo, Japan). To semiquantitate the reticular formation of the epithelium, we measured a more than 10 mm length of the epithelium with a Nexus 6800. The reticular formation was expressed as a percentage of the epithelium without lymphocyte infiltration (normal epithelium). SEM were centered on the ratio of ciliated and nonciliated epithelium. The findings were graded from 0 to 3, defined as follows: grade 0, no ciliated cell; grade 1, the area of ciliated cells was under 30 %; grade 2, the area of ciliated cells was over 30%; grade 3, the area of ciliated cells was over 70%. Bacteriological Study We selected 165 patients from 2 to 15 years of age. Adenoid tissues were cultured immediately after adenoidectomy, and bacterial isolates were identified by aerobic and anaerobic cultures in the bacterial laboratory of the Oita Medical University Hospital (Japan). The bacteriologic findings of middle ear effusions were noted in our previous report [3].
Clinical Study (fig. 1) There was no significant difference between patients with OME and without OME regarding size of the adenoids examined by indirect mirror or flexible fiberscope. The mean A/N ratio was 0.67 ± 0.09 in the patients
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Results
Watanabe/Fujiyoshi/Tomonaga/Mogi
• •
1.0
~•
l7
,.
0 .~
z.... 0.5 «
0
50
O67 . ±0.09
'-' c:
f Ii' t. I::
0.73 ±0.12
~Mean ±SD
••
n =57
n = 28
OME(+)
OME(-)
p < 0.05
(28/59)
40 fi? ai 30
292
(28/59)
a
.OME(+) CJ OME(-) (28/59) (28/59)
Q)
~
E
20 10 0
Sinusitis
Nasal allergy
b
Fig. 1. Clinical study. a A/N ratio. b Incidence of complications.
Histological Study (fig. 2) The mean area of the germinal center was 0.23 ± 0.08 mm 2 in the patients with OME (n = 33), and 0.27 ± 0.1 mm 2 in the patients without
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with OME (n = 57), and 0.73 ± 0.12 in the patients without OME (n = 28). The AlN ratio was significantly lower in the patients with OME than in the patients without OME (p < 0.05). The incidence of sinusitis was 47% in the patients with OME (n = 59), and 28 % in the patients without OME (n = 29). The incidence of sinusitis tended to increase in the patients with OME (p < 0.1). The incidence of nasal allergy was 29% in the patients with OME (n = 58), and 24% in the patients without OME (n = 29). There was no significant difference regarding the incidence of nasal allergy.
29 3
Adenoids and OME
80
•
E 70
a. 50
~
Q)
~ 40
g 30
C
8
20
0..
10
Qi
0
~ ±SD Mean
•
~ 60
...
•
~1'4'
..
(28/59) ±9.50 n = 26
OME(+)
-fF· •
28.4 ± 18.3
..
n=21 p < 0.01
a
OME(-)
30
.OME(+) DOME(-)
rJ)
Q)
~ 20 t.)
15 Qi .c
§ z
(28/59)
10
0
(28/59)
Grade
(28/59)
b
OME (n = 22). There was no significant difference regarding area of germinal center. The mean percentage of normal epithelium was 14.8 ± 9.5% in the patients with OME (n = 26), and 28.4 ± 18.3 % in the patients without OME (n = 21). The percentage of normal epithelium was significantly lower in the patients with OME than in those without it (p < 0.01). That is, reticular epithelium formation was extended in the patients with OME. In the 26 patients with OME, 21 were graded 0 or 1, and 5 were graded 2 or 3, by SEM observation. In the 15 patients without OME, 7 were graded 0 or 1, and 8 were 2 or 3. There was a significant difference between these two groups (p < 0.05). A tendency toward increased stratified squamous epithelium and decreased ciliated epithelium was apparent in patients with OME.
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Fig. 2. Histological study. a Reticular formation. b Ciliated epithelium.
Watanabe/Fujiyoshi/TomonagaiMogi
294
Table 1. Bacteriological study: bacterial isolates from (A) adenoid and from (B) middle ear effusion
A Species
OME (+) (n = 65)
OME (-) (n = 31)
n
%
n
%
H. injluenzae S. pneumoniae S. aureus B. catarrhalis S. pyogenes Others
41 18 15 9 7 54
63.1 27.7 23.1 13.8 10.8 83.1
12 4 11 1 3 24
38.7 12.9 35.5 3.2 9.7 77.4
Positive culture
60 (50 1)/65 = 92.3% (76.9%)
27 (2[1)/31 = 87.1 %(67.7%)
Adenoidectomy (+) (n = 26)
Adenoidectomy (-) (n = 264)
n
%
n
%
H. injluenzae S. pneumoniae S. epidermidis S. aureus B. catarrhalis Others
5 3 2 2 2 3
19.2 11.5 7.7 7.7 7.7 11.5
24 17 17 9 2 11
9.1 6.4 6.4 3.5 0.8 4.1
Positive culture
16 (121)/26 = 61.5% (46.2%)
B
Species
80 (521)/264 = 30.3% (19.7%)
Bacteriological Study (table 1) Haemophilus injluenzae were cultured in 41 adenoid specimens from 65 patients with OME, while 12 of 31 patients without OME were found to have H. injluenzae in their adenoid specimens. There was a significant difference between the patients with OME and without OME (p < 0.05).
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1 Number of ears from which H. injluenzae, S. pneumoniae, B. catarrhalis, and S. aureus were isolated.
Adenoids and OME
295
On the other hand, Streptococcus pneumoniae were cultured in 13 adenoid specimens from 47 patients with OME, while 4 of 23 patients without OME were found to have S. pneumoniae in their adenoid specimens. There was no significant difference between patients with OME and those without OME regarding S. pneumoniae and other species. In the bacteriologic findings of middle ear effusion, the combined number of positive H. injluenzae, S. pneumoniae, Staphylococcus aureus, and Branhamella catarrhalis cultures from OME patients with adenoidectomy was significantly greater than from OME patients without adenoidectmoy (p < 0.01).
In the present study, the adenoid size was somewhat smaller in the patients with OME than in the patients without OME. Roydehouse [4] and Gates et al. [5] could not demonstrate any clinically significant differences in outcome by adenoid size. Our results were the same as those reports. In the histological study, extension of reticular epithelium formation and decreased ciliated epithelium were apparent in patients with OME. These findings suggest an increase of inflammation in the patients with OME. The incidence of sinusitis was higher in the patients with OME than in the patients without OME, and this also supports the increase of inflammation finding. Roukonen et al. [6] emphasized the importance of adenoiditis as a causative agent of OME. Considering these findings, our study suggests that not only adenoid hypertrophy, but also inflammation of the adenoids plays an important role in the pathogenesis of OME. Infection of the nasopharynx and adenoid tissue has been considered a causative factor of OME. It is known that H. injluenzae is an important factor in OME. In our bacteriological study, the incidence of H. injluenzae cultured from adenoids was significantly greater in patients with OME than in patients without OME. And, the incidence of H. injluenzae and other species from the middle ear effusion was significantly greater in patients with adenoidectomy than in patients without adenoidectomy. Our findings suggest that the adenoids play an important role in the etiology of OME by being a reservoir for pathogenic bacteria, and that infection of the adenoid is an important factor in the inflammation of adenoids.
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Discussion
Watanabe/Fujiyoshi/Tomonaga/Mogi
296
References
2 3 4 5
6
Fujiyoshi T, Watanabe T, Ichimiya I, Mogi G: Functional architecture of the nasopharyngeal tonsil. Am J Otolarygol 1989; 10: 124-131. Fujioka M, Young LW, Girdany BR: Radiographic evaluation of adenoidal size in children: Adenoidal-nasopharyngeal ratio. AJR 1979;133:401-404. Tomonaga K, Kurono Y, Chaen T, Mogi G: Adenoids and otitis media with effusion: Nasopharyngeal flora. Am J Otolaryngol 1989;10:204-207. Roydehouse N: A controlled study of adenotonsillectomy. Arch Otolaryngol 1970; 92:611-616. Gates GA, Avery CA, Cooper JC, Prihoda TJ: Chronic secretory otitis media: Effects of surgical management. Ann Otol Rhinol Laryngol 1989;98(suppl 138): 132. Roukonen J, Sandelin K, Makinen J: Adenoids and otitis media with effusion. Ann Otol Rhinol Laryngol 1979;88:166-171.
Goro Mogi, MD, Department of Otolaryngology, Oita Medical University, Hasama-machi, Oita 879-55 (Japan)
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2
Adenoids and Otitis media with Effusion in Children Tetsuo Watanabe, Tatsuya Fujiyoshi, Kazuhiro Tomonaga, GoroMogi Department of Otolaryngology, Oita Medical University, Oita, Japan
Adenoids have long been recognized as an important factor in the pathogenesis of otitis media with effusion (OME). There have been some reports that adenoidectomy was a useful procedure for correction of medically resistant OME. However, there is still much debate about whether the adenoids play an important role in the etiology of OME, and there have been no detailed investigations of the adenoids of patients both with OME and without OME. The purpose of this study is to compare adenoids both with OME and without OME, and to determine whether adenoids may be a cause of OME.
Materials and Methods Over the past 10 years, 171 patients have undergone adenoidectomy under general anesthesia at the Oita Medical University (Japan). Their ages ranged from 0 to 35 years (mean age, 6 years). One hundred and sixty-five of the 171 patients (96%) were from 2 to 15 years old. One hundred and six of those 171 patients had OME; the other 65 did not. In this study, we compared adenoids both with OME and without OME, clinically, histologically, and bacteriologically.
Downloaded by: Université de Paris 193.51.85.197 - 1/22/2020 3:58:06 AM
Clinical Study In the clinical study, we selected 88 patients from 5 to 7 years of age. Fifty-nine of those 88 patients had OME; the other 29 did not have OME. We evaluated the size of adenoids from two perspectives: macroscopic size and relative size. The macroscopic size of the adenoid was examined using an indirect mirror or flexible fiberscope. They were graded from 0 to IV, defined as follows [1]: grade 0, no obvious lymphoid tissue on the posterior wall, including the roof of the nasopharynx, or no enlargement below the level of the superior margin of the choanae; grade I, enlarge-
Adenoids and OME
291
ment reaching the superior margin of the choanae; grade II, enlargement covering one third to one half of the choanae; grade III, enlargement covering one half to two thirds of the choanae; and grade IV, enlargement covering the choanae by more than two thirds. The relative size of adenoids was measured by lateral skull radiography as an adenoidalnasopharyngeal ratio (AIN ratio) obtained by dividing the adenoidal thickness by the nasopharyngeal distance [2]. Also, we examined the incidence of patients who had sinusitis and nasal allergy. Histological Study In the histological study, we selected the same patients as in the clinical study mentioned above for light microscopy. Patients whose ages ranged from 2 to 15 years were selected for scanning electron microscopy (SEM). For light microscopy, adenoids from patients were examined by the standard method: embedded in paraffin and stained with hematoxylin and eosin. The specimens were also placed in Karnovsky's fixative (2.5% glutaraldehyde and 2 % paraformaldehyde in 0.2 M cacodylate buffer pH 7.4) for 2-3 h. Standard methods were used for SEM. Also for SEM, the prefixed tissue specimens were postfixed in buffered 2 %osmium tetraoxide for 2 h ,dehydrated through graded concentrations of ethanol, and dried with t-butyl alcohol. The specimens were coated with gold and examined with a scanning electron microscope (S-800; Hitachi, Tokyo, Japan). Light microscopy was centered on the development of the germinal centers and the reticular formation of the epithelium. To evaluate the development of the germinal centers, we measured the area of the germinal center with a Nexus 6800 image processor (Kashiwagi Research Co. , Tokyo, Japan). To semiquantitate the reticular formation of the epithelium, we measured a more than 10 mm length of the epithelium with a Nexus 6800. The reticular formation was expressed as a percentage of the epithelium without lymphocyte infiltration (normal epithelium). SEM were centered on the ratio of ciliated and nonciliated epithelium. The findings were graded from 0 to 3, defined as follows: grade 0, no ciliated cell; grade 1, the area of ciliated cells was under 30 %; grade 2, the area of ciliated cells was over 30%; grade 3, the area of ciliated cells was over 70%. Bacteriological Study We selected 165 patients from 2 to 15 years of age. Adenoid tissues were cultured immediately after adenoidectomy, and bacterial isolates were identified by aerobic and anaerobic cultures in the bacterial laboratory of the Oita Medical University Hospital (Japan). The bacteriologic findings of middle ear effusions were noted in our previous report [3].
Clinical Study (fig. 1) There was no significant difference between patients with OME and without OME regarding size of the adenoids examined by indirect mirror or flexible fiberscope. The mean A/N ratio was 0.67 ± 0.09 in the patients
Downloaded by: Université de Paris 193.51.85.197 - 1/22/2020 3:58:06 AM
Results
Watanabe/Fujiyoshi/Tomonaga/Mogi
• •
1.0
~•
l7
,.
0 .~
z.... 0.5 «
0
50
O67 . ±0.09
'-' c:
f Ii' t. I::
0.73 ±0.12
~Mean ±SD
••
n =57
n = 28
OME(+)
OME(-)
p < 0.05
(28/59)
40 fi? ai 30
292
(28/59)
a
.OME(+) CJ OME(-) (28/59) (28/59)
Q)
~
E
20 10 0
Sinusitis
Nasal allergy
b
Fig. 1. Clinical study. a A/N ratio. b Incidence of complications.
Histological Study (fig. 2) The mean area of the germinal center was 0.23 ± 0.08 mm 2 in the patients with OME (n = 33), and 0.27 ± 0.1 mm 2 in the patients without
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with OME (n = 57), and 0.73 ± 0.12 in the patients without OME (n = 28). The AlN ratio was significantly lower in the patients with OME than in the patients without OME (p < 0.05). The incidence of sinusitis was 47% in the patients with OME (n = 59), and 28 % in the patients without OME (n = 29). The incidence of sinusitis tended to increase in the patients with OME (p < 0.1). The incidence of nasal allergy was 29% in the patients with OME (n = 58), and 24% in the patients without OME (n = 29). There was no significant difference regarding the incidence of nasal allergy.
29 3
Adenoids and OME
80
•
E 70
a. 50
~
Q)
~ 40
g 30
C
8
20
0..
10
Qi
0
~ ±SD Mean
•
~ 60
...
•
~1'4'
..
(28/59) ±9.50 n = 26
OME(+)
-fF· •
28.4 ± 18.3
..
n=21 p < 0.01
a
OME(-)
30
.OME(+) DOME(-)
rJ)
Q)
~ 20 t.)
15 Qi .c
§ z
(28/59)
10
0
(28/59)
Grade
(28/59)
b
OME (n = 22). There was no significant difference regarding area of germinal center. The mean percentage of normal epithelium was 14.8 ± 9.5% in the patients with OME (n = 26), and 28.4 ± 18.3 % in the patients without OME (n = 21). The percentage of normal epithelium was significantly lower in the patients with OME than in those without it (p < 0.01). That is, reticular epithelium formation was extended in the patients with OME. In the 26 patients with OME, 21 were graded 0 or 1, and 5 were graded 2 or 3, by SEM observation. In the 15 patients without OME, 7 were graded 0 or 1, and 8 were 2 or 3. There was a significant difference between these two groups (p < 0.05). A tendency toward increased stratified squamous epithelium and decreased ciliated epithelium was apparent in patients with OME.
Downloaded by: Université de Paris 193.51.85.197 - 1/22/2020 3:58:06 AM
Fig. 2. Histological study. a Reticular formation. b Ciliated epithelium.
Watanabe/Fujiyoshi/TomonagaiMogi
294
Table 1. Bacteriological study: bacterial isolates from (A) adenoid and from (B) middle ear effusion
A Species
OME (+) (n = 65)
OME (-) (n = 31)
n
%
n
%
H. injluenzae S. pneumoniae S. aureus B. catarrhalis S. pyogenes Others
41 18 15 9 7 54
63.1 27.7 23.1 13.8 10.8 83.1
12 4 11 1 3 24
38.7 12.9 35.5 3.2 9.7 77.4
Positive culture
60 (50 1)/65 = 92.3% (76.9%)
27 (2[1)/31 = 87.1 %(67.7%)
Adenoidectomy (+) (n = 26)
Adenoidectomy (-) (n = 264)
n
%
n
%
H. injluenzae S. pneumoniae S. epidermidis S. aureus B. catarrhalis Others
5 3 2 2 2 3
19.2 11.5 7.7 7.7 7.7 11.5
24 17 17 9 2 11
9.1 6.4 6.4 3.5 0.8 4.1
Positive culture
16 (121)/26 = 61.5% (46.2%)
B
Species
80 (521)/264 = 30.3% (19.7%)
Bacteriological Study (table 1) Haemophilus injluenzae were cultured in 41 adenoid specimens from 65 patients with OME, while 12 of 31 patients without OME were found to have H. injluenzae in their adenoid specimens. There was a significant difference between the patients with OME and without OME (p < 0.05).
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1 Number of ears from which H. injluenzae, S. pneumoniae, B. catarrhalis, and S. aureus were isolated.
Adenoids and OME
295
On the other hand, Streptococcus pneumoniae were cultured in 13 adenoid specimens from 47 patients with OME, while 4 of 23 patients without OME were found to have S. pneumoniae in their adenoid specimens. There was no significant difference between patients with OME and those without OME regarding S. pneumoniae and other species. In the bacteriologic findings of middle ear effusion, the combined number of positive H. injluenzae, S. pneumoniae, Staphylococcus aureus, and Branhamella catarrhalis cultures from OME patients with adenoidectomy was significantly greater than from OME patients without adenoidectmoy (p < 0.01).
In the present study, the adenoid size was somewhat smaller in the patients with OME than in the patients without OME. Roydehouse [4] and Gates et al. [5] could not demonstrate any clinically significant differences in outcome by adenoid size. Our results were the same as those reports. In the histological study, extension of reticular epithelium formation and decreased ciliated epithelium were apparent in patients with OME. These findings suggest an increase of inflammation in the patients with OME. The incidence of sinusitis was higher in the patients with OME than in the patients without OME, and this also supports the increase of inflammation finding. Roukonen et al. [6] emphasized the importance of adenoiditis as a causative agent of OME. Considering these findings, our study suggests that not only adenoid hypertrophy, but also inflammation of the adenoids plays an important role in the pathogenesis of OME. Infection of the nasopharynx and adenoid tissue has been considered a causative factor of OME. It is known that H. injluenzae is an important factor in OME. In our bacteriological study, the incidence of H. injluenzae cultured from adenoids was significantly greater in patients with OME than in patients without OME. And, the incidence of H. injluenzae and other species from the middle ear effusion was significantly greater in patients with adenoidectomy than in patients without adenoidectomy. Our findings suggest that the adenoids play an important role in the etiology of OME by being a reservoir for pathogenic bacteria, and that infection of the adenoid is an important factor in the inflammation of adenoids.
Downloaded by: Université de Paris 193.51.85.197 - 1/22/2020 3:58:06 AM
Discussion
Watanabe/Fujiyoshi/Tomonaga/Mogi
296
References
2 3 4 5
6
Fujiyoshi T, Watanabe T, Ichimiya I, Mogi G: Functional architecture of the nasopharyngeal tonsil. Am J Otolarygol 1989; 10: 124-131. Fujioka M, Young LW, Girdany BR: Radiographic evaluation of adenoidal size in children: Adenoidal-nasopharyngeal ratio. AJR 1979;133:401-404. Tomonaga K, Kurono Y, Chaen T, Mogi G: Adenoids and otitis media with effusion: Nasopharyngeal flora. Am J Otolaryngol 1989;10:204-207. Roydehouse N: A controlled study of adenotonsillectomy. Arch Otolaryngol 1970; 92:611-616. Gates GA, Avery CA, Cooper JC, Prihoda TJ: Chronic secretory otitis media: Effects of surgical management. Ann Otol Rhinol Laryngol 1989;98(suppl 138): 132. Roukonen J, Sandelin K, Makinen J: Adenoids and otitis media with effusion. Ann Otol Rhinol Laryngol 1979;88:166-171.
Goro Mogi, MD, Department of Otolaryngology, Oita Medical University, Hasama-machi, Oita 879-55 (Japan)
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2
