Effects of Recurrent Otitis Media in Infancy on Auditory Perception and Speech MIHA ~ARGI, MD, PhD, AND IRENA H~CEVAR
BOLTE~AR,
MD
Introduction: Recurrent otitis media is commonly encountered in children before 3 years of age. Conductive hearing loss up to 40 dB is frequently associated with suppurative otitis media. Good hearing is believed to be critical to the development of normal language. This study was undertaken to evaluate the effect of recurrent otitis media on auditory perception and speech. Patients and Methods: The experimental group consisted of 33 children with a history of at least three episodes of acute otitis media before 2 years of age. A control group of 29 children experienced one or fewer episodes of otitis media in the first 2 years of age. At the time of investigation, all children were 8 to 10 years of age and had attended similar preschool, kindergarten, and elementary school programs. None showed evidence of mental retardation nor behavioral or emotional disorders. Speech ability was assessed by a battery of tests specific for Slovene language. Subtests of the Wechsler Intelligence Scale for Children were used as well as the Reading and Writing Test. Results: Auditory perception disorders were evident in 88% of children investigated who had a history of at least three episodes of otitis media by 2 years of age. Decreased auditory stimulation during the time of auditory maturation could prevent the development of these functions completely. No statistically significant differences were observed in the development of articulation. These observations underscore the importance of early management of recurrent otitis media during the first 2 years of age. Copyright 0 1992 by W.B. Saunders Company
More than two thirds of children up to age 3 experience at least one episode of acute otitis media, whereas in one third of children the disease recurs three or more times.’ Acute suppurative otitis media is associated with conductive hearing loss up to 40 dB.2S3 In more than one half of the children, effusion in the middle ear cleft persists for several weeks, and in over 10% it persists for longer than 6 months after antimicrobial treatment of acute inflammation. Effusion in the middle ear is most likely to be persistent in children less than 24 months of age. 4,5 In such cases, recurrent acute otitis media can be regarded merely as an exacerbation superimposed on the middle ear effusion. In infants, chronic otitis meFrom the Department of Otorhinolaryngology and Head and Neck Surgery, University of Ljubljana, Ljubljana, Slovenia. Research supported by the Ministry for Science and Technology of the Republic of Slovenia. Address reprint requests to Miha Zargi, MD, Department of Otorhinolaryngology, Head and Neck Surgery, University of Ljubljana, Zaloska 2, 61105 Ljubljana, Slovenia. Copyright 0 1992 by W.B. Saunders Company 0196-0709/92/l SOS-0006$5.00/O 366
American
Journal
of Otolaryngology,
dia with effusion frequently passes unrecognized, especially by pediatricians; therefore, therapists are faced with relatively frequent acute exacerbations. Therefore, in retrospective studies, the two entities cannot be separated with certainty in the majority of cases. Good hearing is known to be one of the basic conditions for normal speech and language development. Children hear speech as a stream of sounds from which basic patterns of language need to be extracted. To enable the children to hear all the acoustic clues of speech adequately, the speech level should at least 18 dB6*7 or 30 dB8 above the background noise level. Accordingly, an already mild or moderate hearing loss can represent a severe impediment. Some investigators suggest that a fluctuating hearing loss creates more problems than a persistent one because the acoustic input is inconsistent. This is the case with recurrent otitis media when hearing level acuity fluctuates as well. 6*gA decreased auditory stimulation during the time of auditory pathway maturation may result in a permanent disturbance of auditory impulse conduction’0311, impaired binaural interaction,l’ and
Vol 13, No 6 (November-December),
1992: pp. 366-372
EFFECTS OF RECURRENT
367
OTITIS MEDIA IN INFANCY
perhaps even in morphological changes of the auditory pathways. This hypothesis has been supported by the findings of several animal evistudies’3-‘” as well as by pathohistologic dence obtained after postmortem central nervous system examination in adults and children with sensorineural hearing 10~s.~~~~~ Several studies point out a correlation between frequent otitis media during the first years of life and later impairment of auditory perception and speech development and also articulation disorders and lower intellectual abilities of the child. Kaplan et al reported impaired verbal ability and lower verbal IQ scores established in a population of Eskimo children with histories of frequent otitis media, e.g., more than three episodes of otitis media in their first 2 years. Also, the children with unimpaired hearing ability at the time of the study presented with worse results in verbal spheres than a group of children without otitis media episodes.lg Lewis has observed deficient auditory sequential memory, decreased auditory discrimination, and the ability to integrate phonemic elements into semantic or syntactic patterns, as well as lower verbal IQ scores, in Australian aborigines’ children with frequently recurring otitis media.” As reported by Zinkus et al, a group of learning-impaired children, who had suffered from chronic otitis media during the first 3 years of life, presented with substantial delays in speech and language development, auditory processing deficits, disturbances in auditory-visual integration, reading disorders, and poorer performance on overall verbal and nonverbal intelligence tests.‘l In children with histories of at least three otitis media episodes, Lehman et al noted retarded verbal development, expressive speech function deficits versus receptive language abilities, and articulation disorders. In all those children, the first episode of otitis media was before 18 months of age.” In a study by Sak and Ruben, children with frequently recurring otitis media before 5 years of age were compared with their disease-free siblings. During the time of investigation, all the children had unimpaired hearing ability. Those with frequent otitis media during infancy were found to have lower verbal and auditory abilities and a lower verbal score on Wechsler’s Intelligence Scale for
Children. 23 In their prosp ective study, Teele et al found significant association between the estimated time with middle ear effusion (MEE) during the first 3 years of life and reduced linguistic ability at 3 years of agez4; significant association was established also for decreased speech and language abilities, school performance, reading disorders, and deficient articulation at 7 years of age. Time spent with MEE after 3 years of age was not a significant predictor of scores on any of the tests administered.25 Results of the studies performed so far differ according to the extent and degree of sequels; also, individual parameters for inclusion of children in the study have not been unified. It was our aim to establish the late sequels of frequent otitis media episodes in infancy (before 2 years of age] on auditory perception and speech development in our conditions. The study was performed in a typical population of Slovenian children who spent a majority of their preschool years in kindergarten. Thus, they received equal (or even optimal) stimulation for their speech and psychomotoric development, although, on the other hand, they were exposed for 8 to 10 hours a day to frequent respiratory infections.
SUBJECTS AND METHODS Subjects The experimental group included 33 children who were treated at the University Department of Otorhinolaryngology and Head and Neck Surgery in Ljubljana at the ages of 0 to 2 years for recurrent acute unilateral or bilateral suppurative otitis media. All the children had histories of at least three episodes of acute otitis media by 2 years of age, whereas 80% of the children had experienced more than six recurrences. Histories were obtained through parental interviews and by review of hospital charts and other medical documentation. In all episodes of acute suppurative otitis media, appropriate antimicrobial agents were administered. Myringotomy was performed in 42 episodes of suppurative otitis media and mastoidectomy in two children. No hearing tests (pure tone audiometry or tympanometry) were made in the experimental group of children before the age of 2 years after the symptoms and signs of suppurative otitis media episode had disappeared. Most of the children were followed up by the pediatricians. A diagnosis of “otitis media with effusion” was never met in medical documentation. No ventilation tubes were inserted. An adenoidectomy was performed in 16
~ARGI AND B~LTE~AR
children (48%) with recurrent episodes of otitis media. After the age of z years, in one fifth of the cases the functioning of the childrens’ middle ears were examined after the treatment of otitis media. The control group was comprised of 28 children; 12 of them had no episodes and the remainder experienced a single episode of otitis media per year in the first 2 years of life (less than five episodes until the time of our investigation). The condition for entry into the control group was absence of conductive hearing loss on pure tone audiometry. The age of the children in both groups at the time of investigation ranged from 8 to 10 years. All of them had spent most of their preschool years in kindergarten, attended regular schooling programs, and did not show evidence of mental retardation or obvious behavioral or emotional disorders. Both groups were matched by age, family size, number of siblings, rank in the family, parents’ education, and socioeconomic status. In the experimental group, there were 20 boys and 13 girls, whereas the control group consisted of 13 boys and 16 girls; the difference was not statistically significant.
Methods The children were examined by an otorhinolaryngologist who assessed the function of their artitular organs as well. Besides pure tone audiometry, tympanometry was performed in children with conductive hearing loss. The criterion for normal hearing was based on the air-conduction threshold results, which had to be at or above the level of 10 dB. Isolated audiometric dips (notches) to 15 dB at not more than one high frequency (6 kHz or 8 kHz) were not considered to be sensorineural hearing loss. Speech abilities and, especially, articulation disorders were assessed by a speech therapist with a battery of conventional tests specific for Slovene language. Five verbal and five nonverbal subtests of Wechsler’s Intelligence Scale for ChildrenRevised (WISC) were usedez6 To detect reading and writing disorders and some auditory processing deficits the Reading & Writing Test according to Sal? was used. Besides the main test, which shows the reading and writing
abilities of a child, it also consists of subtests: sound discrimination, sound discrimination and sequential memory, auditory analysis, and auditory synthesis. They are used to measure the samedifference discrimination skill, phoneme discrimination, auditory sequential memory, and also the child’s ability to integrate phonemic elements into semantic patterns, and their spelling skills. The collected data were processed by means of SPSS/PC+ (SPSS Inc., Chicago, IL). The following analyses from this software program were used: basic statistical description of variables for each group, and analysis of variables with a comparison of both groups (chi-square test, Student’s t-test, variance analysis, non-parametric Mann-Whitney test).
RESULTS Otorhinolaryngological examination was directed into discovering sequels of past otitis media episodes as well as other anatomic and functional disorders that might affect the child’s hearing ability and speech development (Table 1). The results of pure tone audiometry are presented in Table 2. Tympanometry was performed in eight children with conductive hearing loss. There were three cases of type B tympanogram, three cases of type C, and two cases were not conclusive. Parents generally believed that their children had unimpaired hearing. In only four of eight children with conductive hearing loss, were the parents aware of the child’s impairment. Children from the experimental group had their first episode of otitis media at the age of 3 days to 17 months (median 7 months), whereas in those from the control group, the first onset of the disease was noted not earlier than 3 months of age and not later than 22 months of age (median 10 months); the differ-
TABLE 1. Anatomic and Functional Pathological Findings Influencing (N = 33) and Control Group (N = 29) of Children
Hearing Ability and Speech in Experimental
No. of Children Finding Decreased pressure or effusion in the middle ear Chronic perforative otitis media Dental malocclusion Velopharyngeal insufficiency Enlarged adenoids Adenoidectomized children Impaired function of articulation organs
Experimental
5 3 23 0 11 16 0
Group
Control
Group
0 0 20 1 11 5 0
P
.05 -
EFFECTS OF RECURRENT
TABLE 2.
Results
369
OTITIS MEDIA IN INFANCY
of Pure-Tone
Audiometry
in Experimental
and Control
Group
of Children
No. of Children Finding Unilateral or bilateral Unilateral or bilateral Normal hearing Total
Experimental
sensorineural hearing loss conductive or mixed hearing
loss
ence between both groups was statistically significant (P < 0.01). In the preschool period, 11 experimental and 9 control children presented with different speech and articulation disorders: sigmatism, lambdacism, rhotacism, sound substitution, hypernasality, speech rate disorders, and dysfluency. In 9 experimental and 6 control children, treatment by a speech therapist was required. At the time of investigation (ie, at the age of 8 to 10 years), 10 experimental and 5 control children presented with various articulation disorders, such as sigmatism, rhotacism, and hypernasality; the difference between both groups was not statistically significant. WISC test results are presented in Table 3; once again, the difference between both groups was not statistically significant. The results of the Reading & Writing Test according to Sali are presented in Table 4. DISCUSSION In our study, auditory perception disorders were evident in 88% of the children investigated who had a history of at least three episodes of otitis media by 2 years of age. The disorders appeared regardless of the fact that as many as two thirds of these children were attending kindergarten, and thus were not deprived of intensive stimulation for speech and language development. of Wechsler’s Intelligence Scale TABLE 3. Comparison for Children-Revised (WISC) Results in Experimental (N = 33) and Control (N = 29) Group of Children IQ SCORE Experimental
Group
Control
Group
Subtest
X
SD
X
SD
Nonverbal Verbal
112.67 100.85
15.06 12.92
110.86 99.38
12.79 9.00
P -
Group
Control
10 8 15 33
P
Group
-
4 0 25 29
.OOl -
We presume that the hearing level acuity of children with recurrent otitis media from our study was decreased for a remarkable length of time, most probably due to the persistence of MEE. We must admit that in the experimental group of children, the follow-up, especially up to 2 years of age, was far from optimal. Otorhinolaryngologists treated less than one half of the episodes of otitis media; the infants were treated mostly by pediatricians. Otoscopies performed by pediatricians were sometimes questionable; tympanometry was not used and residual effusion was not detected and treated. Decreased auditory stimulation during the time of auditory pathway maturation and development of some specific psychological functions (eg, speech, auditory perception) could prevent the development of these functions from reaching its optimum.‘* In fact, impaired reading and writing skills were more frequent in the experimental group of children than in the control group; however, the difference was not statistically significant. A highly significant difference between both groups was established in auditory sound discrimination and sequential memory, which TABLE 4. Results of Reading & Writing Test According to Sali in Experimental (N = 33) and Control (N = 29) Group of Children No. of Impaired Children Subtest Reading Writing Sound discrimination Sound discrimination and sequential memory Auditory analysis Auditory synthesis
Experimental
Control
Group
Group
P
12 11 29
10 5 6
,000
28 5 7
11 3 4
.OOl -
370
corresponded to the results obtained by Lewis,” Zinkus et al,” Sak and Rubenz3 and Teele et alz5 A problem that we had to face was to find suitable tests that could match the tests used in other studies.1g-25 Slovene language is so different from English that a simple translation of tests would not give us results. One of the rare tests for Slovene-speaking children that shows disorders in the spheres of auditory perception and in reading and writing skills is the Reading & Writing Test created by B. Sali. It is similar to some subtests of the Goldman-Fristoe-Woodcock Auditory Skills Test Battery” and to some subtests of the Illinois Test of Psycholinguistic Abilities.30 Patients having six or more episodes of otitis media before age 6 were termed “otitis prone” by Howie et al 31. Most of the children from the experimental group experienced more than six episodes of otitis media before age 2 and all of them before the age of 6 years. Thus, we could call them “otitis prone” as well. All the children from the experimental group had their first bout of otitis media before the age of 18 months. According to Kaplanlg such an early onset of otitis media episodes could represent a risk factor for recurrent otitis media later in life regardless of the treatment policy used. The investigated children experienced otitis media after the age of z years, but the episodes were less frequent, and in three quarters of the children the episodes ceased after the age of 7 years. We were interested to find out whether the onset of otitis media episodes in our children coincided with their admission to kindergarten, which increased their exposure to respiratory infections. Also, a prolonged disease alone might exert an adverse effect on the child’s development because the child would not be exposed to the stimulatory environment. More than a half of the experimental children had experienced their first otitis media episode before they began to attend kindergarten, whereas only one sixth of the children from the experimental group and one child from the control group had their first onset of the disease within the first month of kindergarten attendance. Therefore, we believe that the onset and development of otitis media depends on the child’s anatomic and
~ARGIAND B~LTE~AR
functional specificities rather than on his exposure to frequent infections. All of the experimental group children had their first otitis media episode before 18 months of age. Lehmann et al” has found delayed speech development, impaired expressive speech abilities, and more frequent articulation disorders in children who experienced their first otitis media episode before the age of 18 months and had at least 3 recurrences. Three quarters of the investigated children had normal hearing ability at the time of investigation, whereas one quarter presented with mild conductive hearing loss and one with moderate hearing loss in one or both ears. Nevertheless, the fact that disorders in auditory processing skills have been found in over four fifths of these children is in agreement with the hypothesis that hearing loss during the first years of life, ie, in the period of central nervous system maturation and speech development, may cause permanent disturbance of auditory perception. When the children with unimpaired hearing ability at the time of investigation were compared with those still affected by hearing loss, no significant difference in auditory perception and speech disorders could be established. In only one half of the eight children with hearing loss were the parents aware of the impairment, which shows the unreliability of anamnestic data. Dobie and Berlin have proved that even a conductive hearing loss of 20 dB results in the loss of morphologic markers that distinguish individual sounds and words from each other.” Listeners with mild to moderate hearing impairment usually have difficulties in discrimination of different fricative and stop consonants inside their own sound classes.” Lehman et a122 attributed the severely defective articulation skills among the majority of children with a history of recurrent otitis media to the fluctuating hearing loss experienced secondary to persisting middle ear effusion. In our study, articulation disorders were found to be twice more frequent in the experimental than in the control group; however, the difference between both groups was not statistically significant. Of the articulation disorders, sigmatism appeared most fre-
EFFECTS OF RECURRENT
371
OTITIS MEDIA IN INFANCY
quently. The latter is often due to dental malocclusion. Although the number of children with malocclusion was practically the same in both groups, there were almost twice as many children with sigmatism found in the investigated group. The difference between our study and the majority of other studies is that both our groups presented with almost equal average verbal and nonverbal IQ scores, which undoubtedly shows that our groups were balanced with respect to the environmental stimulation received. The children included in our study came from an urban environment and had comparable socioeconomic backgrounds. In Slovenia almost every woman is employed, and a large majority of children attend kindergarten. Of the children in our study, all except for one from the study group and one from the control group spent 8 to 10 hours daily in institutions with educational programs that were practically identical throughout Slovenia. Nevertheless, in children with frequent otitis media during their first years of life, the incidence of some auditory processing (sound discrimination and sequential memory) disorders was significantly higher.
CONCLUSION The results of our study have confirmed that frequent otitis media episodes associated with hearing loss adversely affect the child’s auditory processing and most likely also articulation development, although in our series (relatively small) no statistically significant differences have been established in the latter respect. The incidence of disorders was higher in a group of children who had experienced at least three episodes of otitis media by their second year of life. The fact that our results are somehow more favorable than those obtained in other studies can probably be ascribed to the early exposure of our children to a stimulatory environment and not to the efficiency of the diagnostic procedures and treatment of residual or persistent middle ear disease. On the contrary, the study shows that in our conditions, the otorhinolaryngologist should take over the treatment and also the follow-up of children with
recurrent otitis media during the critical period for speech and language development in the first 2 years of life. Prospective studies should answer the question if our understanding of etiology, pathophysiology, and effective treatment of recurrent otitis media and especially otitis media with effusion is adequate to reduce the adverse effects on auditory perception and speech.
REFERENCES 1. Teele DW, Klein JO, Rosner BA: Epidemiology of otitis media in children. Ann Otol Rhino1 Laryngol Suppl 68:5-7, 1980 2. Bluestone CD, Stool SE: Pediatric Otolaryngology. Philadelphia, PA, Saunders, 1983, pp 356-512 3. Paparella MA, Shumrick DA: Otolaryngology. Philadelphia, PA, Saunders, 1980. pp 1381-1509 4. Olmsted RW, Alvarez MC, Moroney JD, et al: The pattern of hearing following acute otitis media. J Pediatr 65:252-255, 1964 5. Shurin PA, Pelton SI, Donner A, et al: Persistence of middle ear effusion after acute otitis media in children. N Engl J Med 300:1121-1123, 1979 6. Skinner M: Effects of peripheral hearing loss on hearing of speech during language acquisition. Semin Speech Lang Hear 3:281-294, 1982 7. Trehub SE, Bull D, Schneider BA: Infants’ detection of speech in noise. J Speech Hear Res 24:202-206, 1981 8. Downs MP: The audiologist and the nonbenign conductive hearing loss of otitis media. Semin Speech Lang Hear 3:295-304, 1982 9. Menyuk P: Development in children with chronic otitis media. Design factors in the assessment of language. Ann Otol Rhino1 Laryngol Suppl 60:78-87, 1979 10. Folsom RC, Weber BA, Thomson G: Auditory brainstem responses in children with early recurrent middle ear disease. Ann Otol Rhino1 Laryngol 92:249-253, 1983 11. Fria TJ, Sabo DL: Auditory brainstem responses in children with otitis media with effusion. Ann Otol Rhino1 Laryngol _ - Suppl 68:200-206, 1980 12. Dobie-i&A, Berlin CI: Influence of otitis media on hearing in development. Ann Otol Rhino1 Laryngol Suppl 60:48-53, 1979 13. Webster DB, Webster M: Neonatal sound deprivation affects brainstem auditory nuclei. Arch Otolaryngol 103:392-396, 1977 14. Webster DB: Effects of neonatal sound deprivation in animal research. Semin Speech Lang Hear 3:336-343, 1982 15. Clopton BM, Silverman MS: Plasticity of binaural interaction. II. Critical period and changes in midline response. J Neurophysiol 40:1275-1280, 1977 16. Silverman MS, Clopton BM: Plasticity of binaural interaction. I. Effect of early auditory deprivation. J Neurophysiol 40:1266-1274, 1977 17. Lawrence M, Johnsson L: The role of the organ of Corti in auditory nerve stimulation. Ann Otol Rhino1 Laryngol 82:464-472, 1973 18. Otte J, Schuknecht H, Kerr A: Ganglion cell populations in normal and pathological human cochleaimplications for cochlear implantation. Laryngoscope 88: 1231-1246, 1978
372
19. Kaplan GJ, Fleshman JK, Bender TR, et al: Longterm effects of otitis media. A ten-year cohort study of Alaskan Eskimo children. Pediatrics 52:577-585, 1973 20. Lewis N: Otitis media and linguistic incompetence. Arch Otolaryngol Head Neck Surg 102:387-390, 1976 21. Zinkus PW, Gottlieb MI, Schapiro M: Developmental and psychoeducational sequelae of chronic otitis media. Am J Dis Child 132:1100-1104,1978 22. Lehmann MD, Charron K, Kummer A, et al: The effect of chronic middle ear effusion on speech and language development. A descriptive study. Int J Pediatr Otorhinolaryngol 1:137-144, 1979 23. Sak R, Ruben R: Effects of recurrent middle ear effusion in preschool years on language and learning. J Dev Behav Pediatr 3:7-11, 1982 24. Teele DW, Klein JO, Rosner BA, et al: Otitis media with effusion during the first three years of life and development of speech and language. Pediatrics 74:282-287, 1984 25. Teele DW, Klein JO, Chase C, et al: Otitis media in
ZARGI
ANDI~OLTE~AR
infancy and intellectual ability, school achievement, speech and language at age 7 years. J Infect Dis 162:685694,199O 26. Sali B: Wechslerjev test inteligentnosti za otrokeWISC. Popravljena oblika. Ljubljana, Zavod SRS za produktivnost dela Ljubljana, 1974 27. Sali B: Motnje v branju in pisanju, Ljubljana, Zavod SR Slovenije za rehabilitacijo invalidov Ljubljana, 1975 28. Clark JG: The effects of middle ear disease on early child development. A literature review. Semin Speech Lang Hear 1:149-156, 1980 29. Kirk SA, McCarthy JP, Kirk WD: The Illinois test of psycholinguistic abilities (ed 2). Urbana, IL, University of Illinois Press, 1968 36. Woodcock R: Goldman-Fristoe-Woodcock auditory skills test battery-technical manual. Circle Pines, MN, American Guidance Service, 1976 31. Howie VM, Ploussard JH, Sloyer J: The “otitisprone” condition. Am J Dis Child 129:676-678, 1975
BOLTE~AR,
MD
Introduction: Recurrent otitis media is commonly encountered in children before 3 years of age. Conductive hearing loss up to 40 dB is frequently associated with suppurative otitis media. Good hearing is believed to be critical to the development of normal language. This study was undertaken to evaluate the effect of recurrent otitis media on auditory perception and speech. Patients and Methods: The experimental group consisted of 33 children with a history of at least three episodes of acute otitis media before 2 years of age. A control group of 29 children experienced one or fewer episodes of otitis media in the first 2 years of age. At the time of investigation, all children were 8 to 10 years of age and had attended similar preschool, kindergarten, and elementary school programs. None showed evidence of mental retardation nor behavioral or emotional disorders. Speech ability was assessed by a battery of tests specific for Slovene language. Subtests of the Wechsler Intelligence Scale for Children were used as well as the Reading and Writing Test. Results: Auditory perception disorders were evident in 88% of children investigated who had a history of at least three episodes of otitis media by 2 years of age. Decreased auditory stimulation during the time of auditory maturation could prevent the development of these functions completely. No statistically significant differences were observed in the development of articulation. These observations underscore the importance of early management of recurrent otitis media during the first 2 years of age. Copyright 0 1992 by W.B. Saunders Company
More than two thirds of children up to age 3 experience at least one episode of acute otitis media, whereas in one third of children the disease recurs three or more times.’ Acute suppurative otitis media is associated with conductive hearing loss up to 40 dB.2S3 In more than one half of the children, effusion in the middle ear cleft persists for several weeks, and in over 10% it persists for longer than 6 months after antimicrobial treatment of acute inflammation. Effusion in the middle ear is most likely to be persistent in children less than 24 months of age. 4,5 In such cases, recurrent acute otitis media can be regarded merely as an exacerbation superimposed on the middle ear effusion. In infants, chronic otitis meFrom the Department of Otorhinolaryngology and Head and Neck Surgery, University of Ljubljana, Ljubljana, Slovenia. Research supported by the Ministry for Science and Technology of the Republic of Slovenia. Address reprint requests to Miha Zargi, MD, Department of Otorhinolaryngology, Head and Neck Surgery, University of Ljubljana, Zaloska 2, 61105 Ljubljana, Slovenia. Copyright 0 1992 by W.B. Saunders Company 0196-0709/92/l SOS-0006$5.00/O 366
American
Journal
of Otolaryngology,
dia with effusion frequently passes unrecognized, especially by pediatricians; therefore, therapists are faced with relatively frequent acute exacerbations. Therefore, in retrospective studies, the two entities cannot be separated with certainty in the majority of cases. Good hearing is known to be one of the basic conditions for normal speech and language development. Children hear speech as a stream of sounds from which basic patterns of language need to be extracted. To enable the children to hear all the acoustic clues of speech adequately, the speech level should at least 18 dB6*7 or 30 dB8 above the background noise level. Accordingly, an already mild or moderate hearing loss can represent a severe impediment. Some investigators suggest that a fluctuating hearing loss creates more problems than a persistent one because the acoustic input is inconsistent. This is the case with recurrent otitis media when hearing level acuity fluctuates as well. 6*gA decreased auditory stimulation during the time of auditory pathway maturation may result in a permanent disturbance of auditory impulse conduction’0311, impaired binaural interaction,l’ and
Vol 13, No 6 (November-December),
1992: pp. 366-372
EFFECTS OF RECURRENT
367
OTITIS MEDIA IN INFANCY
perhaps even in morphological changes of the auditory pathways. This hypothesis has been supported by the findings of several animal evistudies’3-‘” as well as by pathohistologic dence obtained after postmortem central nervous system examination in adults and children with sensorineural hearing 10~s.~~~~~ Several studies point out a correlation between frequent otitis media during the first years of life and later impairment of auditory perception and speech development and also articulation disorders and lower intellectual abilities of the child. Kaplan et al reported impaired verbal ability and lower verbal IQ scores established in a population of Eskimo children with histories of frequent otitis media, e.g., more than three episodes of otitis media in their first 2 years. Also, the children with unimpaired hearing ability at the time of the study presented with worse results in verbal spheres than a group of children without otitis media episodes.lg Lewis has observed deficient auditory sequential memory, decreased auditory discrimination, and the ability to integrate phonemic elements into semantic or syntactic patterns, as well as lower verbal IQ scores, in Australian aborigines’ children with frequently recurring otitis media.” As reported by Zinkus et al, a group of learning-impaired children, who had suffered from chronic otitis media during the first 3 years of life, presented with substantial delays in speech and language development, auditory processing deficits, disturbances in auditory-visual integration, reading disorders, and poorer performance on overall verbal and nonverbal intelligence tests.‘l In children with histories of at least three otitis media episodes, Lehman et al noted retarded verbal development, expressive speech function deficits versus receptive language abilities, and articulation disorders. In all those children, the first episode of otitis media was before 18 months of age.” In a study by Sak and Ruben, children with frequently recurring otitis media before 5 years of age were compared with their disease-free siblings. During the time of investigation, all the children had unimpaired hearing ability. Those with frequent otitis media during infancy were found to have lower verbal and auditory abilities and a lower verbal score on Wechsler’s Intelligence Scale for
Children. 23 In their prosp ective study, Teele et al found significant association between the estimated time with middle ear effusion (MEE) during the first 3 years of life and reduced linguistic ability at 3 years of agez4; significant association was established also for decreased speech and language abilities, school performance, reading disorders, and deficient articulation at 7 years of age. Time spent with MEE after 3 years of age was not a significant predictor of scores on any of the tests administered.25 Results of the studies performed so far differ according to the extent and degree of sequels; also, individual parameters for inclusion of children in the study have not been unified. It was our aim to establish the late sequels of frequent otitis media episodes in infancy (before 2 years of age] on auditory perception and speech development in our conditions. The study was performed in a typical population of Slovenian children who spent a majority of their preschool years in kindergarten. Thus, they received equal (or even optimal) stimulation for their speech and psychomotoric development, although, on the other hand, they were exposed for 8 to 10 hours a day to frequent respiratory infections.
SUBJECTS AND METHODS Subjects The experimental group included 33 children who were treated at the University Department of Otorhinolaryngology and Head and Neck Surgery in Ljubljana at the ages of 0 to 2 years for recurrent acute unilateral or bilateral suppurative otitis media. All the children had histories of at least three episodes of acute otitis media by 2 years of age, whereas 80% of the children had experienced more than six recurrences. Histories were obtained through parental interviews and by review of hospital charts and other medical documentation. In all episodes of acute suppurative otitis media, appropriate antimicrobial agents were administered. Myringotomy was performed in 42 episodes of suppurative otitis media and mastoidectomy in two children. No hearing tests (pure tone audiometry or tympanometry) were made in the experimental group of children before the age of 2 years after the symptoms and signs of suppurative otitis media episode had disappeared. Most of the children were followed up by the pediatricians. A diagnosis of “otitis media with effusion” was never met in medical documentation. No ventilation tubes were inserted. An adenoidectomy was performed in 16
~ARGI AND B~LTE~AR
children (48%) with recurrent episodes of otitis media. After the age of z years, in one fifth of the cases the functioning of the childrens’ middle ears were examined after the treatment of otitis media. The control group was comprised of 28 children; 12 of them had no episodes and the remainder experienced a single episode of otitis media per year in the first 2 years of life (less than five episodes until the time of our investigation). The condition for entry into the control group was absence of conductive hearing loss on pure tone audiometry. The age of the children in both groups at the time of investigation ranged from 8 to 10 years. All of them had spent most of their preschool years in kindergarten, attended regular schooling programs, and did not show evidence of mental retardation or obvious behavioral or emotional disorders. Both groups were matched by age, family size, number of siblings, rank in the family, parents’ education, and socioeconomic status. In the experimental group, there were 20 boys and 13 girls, whereas the control group consisted of 13 boys and 16 girls; the difference was not statistically significant.
Methods The children were examined by an otorhinolaryngologist who assessed the function of their artitular organs as well. Besides pure tone audiometry, tympanometry was performed in children with conductive hearing loss. The criterion for normal hearing was based on the air-conduction threshold results, which had to be at or above the level of 10 dB. Isolated audiometric dips (notches) to 15 dB at not more than one high frequency (6 kHz or 8 kHz) were not considered to be sensorineural hearing loss. Speech abilities and, especially, articulation disorders were assessed by a speech therapist with a battery of conventional tests specific for Slovene language. Five verbal and five nonverbal subtests of Wechsler’s Intelligence Scale for ChildrenRevised (WISC) were usedez6 To detect reading and writing disorders and some auditory processing deficits the Reading & Writing Test according to Sal? was used. Besides the main test, which shows the reading and writing
abilities of a child, it also consists of subtests: sound discrimination, sound discrimination and sequential memory, auditory analysis, and auditory synthesis. They are used to measure the samedifference discrimination skill, phoneme discrimination, auditory sequential memory, and also the child’s ability to integrate phonemic elements into semantic patterns, and their spelling skills. The collected data were processed by means of SPSS/PC+ (SPSS Inc., Chicago, IL). The following analyses from this software program were used: basic statistical description of variables for each group, and analysis of variables with a comparison of both groups (chi-square test, Student’s t-test, variance analysis, non-parametric Mann-Whitney test).
RESULTS Otorhinolaryngological examination was directed into discovering sequels of past otitis media episodes as well as other anatomic and functional disorders that might affect the child’s hearing ability and speech development (Table 1). The results of pure tone audiometry are presented in Table 2. Tympanometry was performed in eight children with conductive hearing loss. There were three cases of type B tympanogram, three cases of type C, and two cases were not conclusive. Parents generally believed that their children had unimpaired hearing. In only four of eight children with conductive hearing loss, were the parents aware of the child’s impairment. Children from the experimental group had their first episode of otitis media at the age of 3 days to 17 months (median 7 months), whereas in those from the control group, the first onset of the disease was noted not earlier than 3 months of age and not later than 22 months of age (median 10 months); the differ-
TABLE 1. Anatomic and Functional Pathological Findings Influencing (N = 33) and Control Group (N = 29) of Children
Hearing Ability and Speech in Experimental
No. of Children Finding Decreased pressure or effusion in the middle ear Chronic perforative otitis media Dental malocclusion Velopharyngeal insufficiency Enlarged adenoids Adenoidectomized children Impaired function of articulation organs
Experimental
5 3 23 0 11 16 0
Group
Control
Group
0 0 20 1 11 5 0
P
.05 -
EFFECTS OF RECURRENT
TABLE 2.
Results
369
OTITIS MEDIA IN INFANCY
of Pure-Tone
Audiometry
in Experimental
and Control
Group
of Children
No. of Children Finding Unilateral or bilateral Unilateral or bilateral Normal hearing Total
Experimental
sensorineural hearing loss conductive or mixed hearing
loss
ence between both groups was statistically significant (P < 0.01). In the preschool period, 11 experimental and 9 control children presented with different speech and articulation disorders: sigmatism, lambdacism, rhotacism, sound substitution, hypernasality, speech rate disorders, and dysfluency. In 9 experimental and 6 control children, treatment by a speech therapist was required. At the time of investigation (ie, at the age of 8 to 10 years), 10 experimental and 5 control children presented with various articulation disorders, such as sigmatism, rhotacism, and hypernasality; the difference between both groups was not statistically significant. WISC test results are presented in Table 3; once again, the difference between both groups was not statistically significant. The results of the Reading & Writing Test according to Sali are presented in Table 4. DISCUSSION In our study, auditory perception disorders were evident in 88% of the children investigated who had a history of at least three episodes of otitis media by 2 years of age. The disorders appeared regardless of the fact that as many as two thirds of these children were attending kindergarten, and thus were not deprived of intensive stimulation for speech and language development. of Wechsler’s Intelligence Scale TABLE 3. Comparison for Children-Revised (WISC) Results in Experimental (N = 33) and Control (N = 29) Group of Children IQ SCORE Experimental
Group
Control
Group
Subtest
X
SD
X
SD
Nonverbal Verbal
112.67 100.85
15.06 12.92
110.86 99.38
12.79 9.00
P -
Group
Control
10 8 15 33
P
Group
-
4 0 25 29
.OOl -
We presume that the hearing level acuity of children with recurrent otitis media from our study was decreased for a remarkable length of time, most probably due to the persistence of MEE. We must admit that in the experimental group of children, the follow-up, especially up to 2 years of age, was far from optimal. Otorhinolaryngologists treated less than one half of the episodes of otitis media; the infants were treated mostly by pediatricians. Otoscopies performed by pediatricians were sometimes questionable; tympanometry was not used and residual effusion was not detected and treated. Decreased auditory stimulation during the time of auditory pathway maturation and development of some specific psychological functions (eg, speech, auditory perception) could prevent the development of these functions from reaching its optimum.‘* In fact, impaired reading and writing skills were more frequent in the experimental group of children than in the control group; however, the difference was not statistically significant. A highly significant difference between both groups was established in auditory sound discrimination and sequential memory, which TABLE 4. Results of Reading & Writing Test According to Sali in Experimental (N = 33) and Control (N = 29) Group of Children No. of Impaired Children Subtest Reading Writing Sound discrimination Sound discrimination and sequential memory Auditory analysis Auditory synthesis
Experimental
Control
Group
Group
P
12 11 29
10 5 6
,000
28 5 7
11 3 4
.OOl -
370
corresponded to the results obtained by Lewis,” Zinkus et al,” Sak and Rubenz3 and Teele et alz5 A problem that we had to face was to find suitable tests that could match the tests used in other studies.1g-25 Slovene language is so different from English that a simple translation of tests would not give us results. One of the rare tests for Slovene-speaking children that shows disorders in the spheres of auditory perception and in reading and writing skills is the Reading & Writing Test created by B. Sali. It is similar to some subtests of the Goldman-Fristoe-Woodcock Auditory Skills Test Battery” and to some subtests of the Illinois Test of Psycholinguistic Abilities.30 Patients having six or more episodes of otitis media before age 6 were termed “otitis prone” by Howie et al 31. Most of the children from the experimental group experienced more than six episodes of otitis media before age 2 and all of them before the age of 6 years. Thus, we could call them “otitis prone” as well. All the children from the experimental group had their first bout of otitis media before the age of 18 months. According to Kaplanlg such an early onset of otitis media episodes could represent a risk factor for recurrent otitis media later in life regardless of the treatment policy used. The investigated children experienced otitis media after the age of z years, but the episodes were less frequent, and in three quarters of the children the episodes ceased after the age of 7 years. We were interested to find out whether the onset of otitis media episodes in our children coincided with their admission to kindergarten, which increased their exposure to respiratory infections. Also, a prolonged disease alone might exert an adverse effect on the child’s development because the child would not be exposed to the stimulatory environment. More than a half of the experimental children had experienced their first otitis media episode before they began to attend kindergarten, whereas only one sixth of the children from the experimental group and one child from the control group had their first onset of the disease within the first month of kindergarten attendance. Therefore, we believe that the onset and development of otitis media depends on the child’s anatomic and
~ARGIAND B~LTE~AR
functional specificities rather than on his exposure to frequent infections. All of the experimental group children had their first otitis media episode before 18 months of age. Lehmann et al” has found delayed speech development, impaired expressive speech abilities, and more frequent articulation disorders in children who experienced their first otitis media episode before the age of 18 months and had at least 3 recurrences. Three quarters of the investigated children had normal hearing ability at the time of investigation, whereas one quarter presented with mild conductive hearing loss and one with moderate hearing loss in one or both ears. Nevertheless, the fact that disorders in auditory processing skills have been found in over four fifths of these children is in agreement with the hypothesis that hearing loss during the first years of life, ie, in the period of central nervous system maturation and speech development, may cause permanent disturbance of auditory perception. When the children with unimpaired hearing ability at the time of investigation were compared with those still affected by hearing loss, no significant difference in auditory perception and speech disorders could be established. In only one half of the eight children with hearing loss were the parents aware of the impairment, which shows the unreliability of anamnestic data. Dobie and Berlin have proved that even a conductive hearing loss of 20 dB results in the loss of morphologic markers that distinguish individual sounds and words from each other.” Listeners with mild to moderate hearing impairment usually have difficulties in discrimination of different fricative and stop consonants inside their own sound classes.” Lehman et a122 attributed the severely defective articulation skills among the majority of children with a history of recurrent otitis media to the fluctuating hearing loss experienced secondary to persisting middle ear effusion. In our study, articulation disorders were found to be twice more frequent in the experimental than in the control group; however, the difference between both groups was not statistically significant. Of the articulation disorders, sigmatism appeared most fre-
EFFECTS OF RECURRENT
371
OTITIS MEDIA IN INFANCY
quently. The latter is often due to dental malocclusion. Although the number of children with malocclusion was practically the same in both groups, there were almost twice as many children with sigmatism found in the investigated group. The difference between our study and the majority of other studies is that both our groups presented with almost equal average verbal and nonverbal IQ scores, which undoubtedly shows that our groups were balanced with respect to the environmental stimulation received. The children included in our study came from an urban environment and had comparable socioeconomic backgrounds. In Slovenia almost every woman is employed, and a large majority of children attend kindergarten. Of the children in our study, all except for one from the study group and one from the control group spent 8 to 10 hours daily in institutions with educational programs that were practically identical throughout Slovenia. Nevertheless, in children with frequent otitis media during their first years of life, the incidence of some auditory processing (sound discrimination and sequential memory) disorders was significantly higher.
CONCLUSION The results of our study have confirmed that frequent otitis media episodes associated with hearing loss adversely affect the child’s auditory processing and most likely also articulation development, although in our series (relatively small) no statistically significant differences have been established in the latter respect. The incidence of disorders was higher in a group of children who had experienced at least three episodes of otitis media by their second year of life. The fact that our results are somehow more favorable than those obtained in other studies can probably be ascribed to the early exposure of our children to a stimulatory environment and not to the efficiency of the diagnostic procedures and treatment of residual or persistent middle ear disease. On the contrary, the study shows that in our conditions, the otorhinolaryngologist should take over the treatment and also the follow-up of children with
recurrent otitis media during the critical period for speech and language development in the first 2 years of life. Prospective studies should answer the question if our understanding of etiology, pathophysiology, and effective treatment of recurrent otitis media and especially otitis media with effusion is adequate to reduce the adverse effects on auditory perception and speech.
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19. Kaplan GJ, Fleshman JK, Bender TR, et al: Longterm effects of otitis media. A ten-year cohort study of Alaskan Eskimo children. Pediatrics 52:577-585, 1973 20. Lewis N: Otitis media and linguistic incompetence. Arch Otolaryngol Head Neck Surg 102:387-390, 1976 21. Zinkus PW, Gottlieb MI, Schapiro M: Developmental and psychoeducational sequelae of chronic otitis media. Am J Dis Child 132:1100-1104,1978 22. Lehmann MD, Charron K, Kummer A, et al: The effect of chronic middle ear effusion on speech and language development. A descriptive study. Int J Pediatr Otorhinolaryngol 1:137-144, 1979 23. Sak R, Ruben R: Effects of recurrent middle ear effusion in preschool years on language and learning. J Dev Behav Pediatr 3:7-11, 1982 24. Teele DW, Klein JO, Rosner BA, et al: Otitis media with effusion during the first three years of life and development of speech and language. Pediatrics 74:282-287, 1984 25. Teele DW, Klein JO, Chase C, et al: Otitis media in
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infancy and intellectual ability, school achievement, speech and language at age 7 years. J Infect Dis 162:685694,199O 26. Sali B: Wechslerjev test inteligentnosti za otrokeWISC. Popravljena oblika. Ljubljana, Zavod SRS za produktivnost dela Ljubljana, 1974 27. Sali B: Motnje v branju in pisanju, Ljubljana, Zavod SR Slovenije za rehabilitacijo invalidov Ljubljana, 1975 28. Clark JG: The effects of middle ear disease on early child development. A literature review. Semin Speech Lang Hear 1:149-156, 1980 29. Kirk SA, McCarthy JP, Kirk WD: The Illinois test of psycholinguistic abilities (ed 2). Urbana, IL, University of Illinois Press, 1968 36. Woodcock R: Goldman-Fristoe-Woodcock auditory skills test battery-technical manual. Circle Pines, MN, American Guidance Service, 1976 31. Howie VM, Ploussard JH, Sloyer J: The “otitisprone” condition. Am J Dis Child 129:676-678, 1975
