Abstract
Objective: This article, through a summary of the current literature available, studies the relationship between recurrent otitis media (OM) and communication (speech and language) and educational development. Areas discussed include historical and current views of their relationship, hearing loss and auditory abilities, language and speech development, and educational (cognitive and academic) performance of children with histories of OM. As well, the authors present a model for the use of physicians, communications specialists, and educators when dealing with such children.
Conclusion: Despite significant advances in our understanding of OM-related communication and educational development, more prospective studies that also consider the role of other mediating and moderating variables affecting language in children with OM histories are needed.
Sommaire
Objectif. Cet article, par le biais d'un resume de la litterature actuelle disponible, etudie le rapport entre l'otite moyenne recurrente et le developpement tant de la communication (langage et parole) que de l'education. Les sujets discutes comprennent les perspectives historiques et actuelles sur ces relations, la surdite et les capacites auditives, le developpement du langage et de la parole, de meme que les performances educationnelles (cognitives et acad6miques) d'enfants avec antecedents d'otite moyenne. De plus, les auteurs presentent un modele a l'usage des medecins, des specialistes de l'education et des educateurs lorsqu'ils doivent s'occuper de tels enfants.
Conclusion: Malgre des progres significatifs dans notre comprehension du developpement de la communication et de l'6ducation en relation avec l'otite moyenne, d'autres etudes prospectives sont requises qui considereront aussi le role de variables autres qui s'interposent, qui temperent et qui affectent le langage chez les enfants avec antecedent d'otite moyenne.
Key words: academic performance, attention, behaviour, central auditory processing disorder, expressive langage, hearing, otitis media, receptive language, speech perception, speech production
Consensus has not been reached on the influence of recurrent otitis media (OM) on communication development. The interest in OM and child development has certainly not waned; indeed, it remains as strong at the end of this millennium as it was 30 years ago. Any association between certain developmental outcomes and a history of early OM is relevant to medical practitioners, audiologists, speech-language pathologists, psychologists, and educators, as well as to formulators of public health care policy and the scientific community. The approach to the study of OM and child development has changed appreciably from that of previous years. Now, research designs specifically address complex developmental questions using appropriate methodologies that account for the natural history of the disease, the hearing loss accompanying the condition, and the numerous variables that influence outcome.
Since OM is frequently associated with some degree of conductive hearing loss in early life, an important question is whether or not a 'critical' or `sensitive' period for auditory development exists in humans. A parallel issue is whether or not the hearing loss associated with OM represents a form of `early auditory deprivation.' The anatomic, physiologic, and behavioral sequelae demonstrated through studies of imposed auditory deprivation in animals are suggestive, but neither can the results be directly applied to humans,l nor have the fluctuant hearing impairments and environmental circumstances experienced by children with OM been replicable in animal research.l Some argue that even if an auditory deprivation of some sort did occur as a result of persistent early OM and hearing loss, both the proportionately greater normal auditory input children receive and/or neural plasticity would obviate any early deficits once the OM had subsided.2 To date, neither of these fundamental issues has been examined through empiric study of humans.
A Model of the Effects of Otitis Media on Development
Figure 1 presents our working model of OM, the development of communication, and later academic achievement. The model is based on our understanding and interpretation of the current literature on OM and other areas of child development. Note that throughout this article, we have chosen to use the general term `otitis media' (OM) since some studies have not clearly distinguished between ears having acute otitis media (AOM) and those having otitis media with effusion (OME). As is seen in this model, we consider the peripheral hearing loss associated with OM to be the primary factor that mediates communication development. Other variables, such as the general malaise sometimes associated with recurrent OM, have been suggested as accounting for some developmental problems.2 While potentially moderating outcome, malaise as a primary factor does not, in our opinion, account for the auditory sequelae (discussed later) associated with early OM, nor does it fit with the observation that about half of all cases of OM are silent.3 Our model does recognize that linguistic, auditory, and other parent-child factors have major mediating roles in the study of the effect of OM on outcome.
Based on current data, we consider the early conductive hearing loss associated with OM in some children to be a type of early auditory deprivation (degree-, duration-, and age-of-onset-dependent). This view is supported by increasing amounts of empiric evidence. For example, some studies have found that a history of OM-associated hearing loss affects basic auditory processes, such as binaural hearing.4-7 In older children, experience with normal auditory input (after the insertion of ventilating tubes) was shown to result in a resolution of atypical auditory indices (smaller-thantypical masking-level differences) in most but not all subjects.47 Our model contends that when such atypical auditory experiences occur early in infancy, young children in the earliest stages of the development of auditory processes are at greater risk for sequelae than are older children who experience similar impairments. Thus, functional communication consequences could result despite 'resolution' of specific auditory skills because of the stage of development at which OM and the specific auditory sequelae first occurred.
Degraded and reduced auditory-linguistic experiences (from hearing loss or from a less-than-optimal language environment) could result in an aberrant representation of the acoustic-phonetic code of the child's native language. In addition, lack of attention to spoken language (a pattern or habit developed over time) in combination with reduced auditory sensitivity may compromise the development of the young child's phonologic working memory, an important precursor to the development of his or her lexicon. As sounds are used in words grammatically (syntax), hearing loss and inattention may cause the young child to miss important but subtle morphologic markers such as speechsounds that denote plurality (Is/), possession (Is/), and past tense ( -ed). These morphemes are low in intensity, high in frequency, and occur at the end of words, all attributes that make them particularly vulnerable. Such deficits may or may not manifest themselves as delays in expressive or receptive language when standardized, global measures of language are employed.
A limited vocabulary and reduced syntactic complexity may later affect the child's abilities to organize discourse and produce narratives. These skills, important to educational achievement, require facility with auditory memory, recall, syntax, and vocabulary.89 Evidence exists that such complex language-processing and attention abilities may be poorer in children with early OM histories than in those children without.s10 Selective listening skills that are attention dependent may also be challenged, such as when a primary message must be recognized in the presence of background competition,ll-"3 or when speech is presented at lower intensities than average conversational levels.l4
This view of the effects of OM on development is not fundamentally different from those of years past. However, the current model does acknowledge the powerful influences of mediating and moderating variables such as the environment, parent-child interactions, language experiences, and most importantly, hearing on outcome. Further, the usefulness of the model in explaining the consequences of OM is now being supported by well-conducted clinical research.
Historical Views on Otitis Media and Child Development
In 1980, the seminal papers of Ventryl9 and Paradise2 refocused the way that clinical researchers studied possible developmental sequelae resulting from OM. Prior to the publication of these critiques, the investigations that examined auditory, language, and educational outcomes and OM were flawed by their methodologic approaches. After publication of the Ventry and Paradise articles, a new standard was set by which all subsequent studies would be judged. Briefly, Ventry and Paradise criticized the following procedures:
1. Use of retrospective rather than prospective research designs. Prospective studies allow an accurate history of OM to be obtained. Young subjects can then be categorized based on direct observation of the disease process rather than by parent report or medical history.
2. Lack of information about hearing. Without audiometric assessment, any relationships between hearing and outcome could not be established.
3. Infrequent use of age-appropriate, standardized, sensitive, and specific tests. These include tools and procedures to identify OM in infants and children, as well as measures of global and specific language, speech, and cognitive behaviours.
4. Use of biased observers. Testers were often aware of the OM status of children under study; examiner bias may have affected outcomes.
5. Use of restricted subject groups. Cohorts were often already at risk for developmental problems, or were of restricted or specific backgrounds making application of results to the general population difficult.
6. Failure to study children at more than one age or on more than one measure. Lack of longitudinal follow-up and limited testing in only one dimension prohibited a developmental view of OM sequelae.
Roberts and Wallacel6 recently undertook a comprehensive review of language and OM finding over 75 studies published on the topic since the mid-1960s. Despite this sizable body of literature on language and speech, meta-analyses for the development of the Guidelines for the Management of Otitis Media with Effusionl7 through the U.S. Department of Health and Human Service's Agency for Health Care Policy and Research (AHCPR) were not possible because of wide variations in study designs. In general, Roberts and Wallace reported that this total body of literature on OM and language development was essentially equivocal. One group of studies suggested that children with OM histories had significantly lower scores on measures of receptive and expressive language, as well as speech production, than did their OM-free peers. However, another group of investigations failed to find any relationship between OM history and the aforementioned communication skills. Thus, the existing literature on language and speech development left the topic open for debate, and confusion persisted about whether or not otitis media in early life ought be a concern to clinicians, educators, and parents alike.
There have been similar questions regarding the effects of OM on cognition and educational performance. Wallace and Hooper"8 reviewed the findings of nine retrospective studies that examined the association between OM and cognition '(intellectual functioning). Some of the investigations found children with OM histories to have significantly lower scores, a different pattern of scores, or both on cognitive measures compared to their OM-free peers. The cross-sectional study of Kaplan and colleaguesl9 found a relationship between lower cognitive scores and audiometric thresholds that were measured at the time of IQ testing. Another study by Sak and Ruben20 found only verbal (not overall or performance) IQ scores differed among OM-positive and OM-free sibling pairs. Thus, the majority of studies that used a retrospective design suggested that a history of OM negatively influenced intellectual function. Similarly, Wallace and Hooper"8 found that the majority of retrospective studies on academic achievement reported that reading, spelling, and mathematics skills were negatively influenced by OM. Others found that discrepancies between academic achievement and grade level were also associated with the condition. Several cross-sectional studies compared children with and without tympanometric or otoscopic evidence of OM. Children previously diagnosed with learning disabilities were found more likely to have abnormal tympanograms than were typically learning peers. Similarly, those classified in school as `poor readers' were more likely to have abnormal otoscopic findings than were children considered to be typical readers.
As was true of the area of language and speech, these retrospective and cross-sectional studies of cognition and academic performance were useful in suggesting areas of potential concern, but they were not compelling as support for the existence of sequelae (such as learning disabilities). Again, inherent methodologic flaws failed to allow practitioners and parents to be convinced that there was any long-term harm associated with OM. In general, there has been low regard for the literature on OM and child development, and debate over the existence of developmental sequelae was often supported by anecdotes and experiences rather than strong empiric evidence.
Current Views on the Influence of Otitis Media on Outcome
It now appears that we have `turned the corner' with regard to how clinical researchers address the important issues of child development and OM. Today's studies are, in the main, prospective in design. Most investigators involved in OM research carefully and periodically document the presence or absence of middle-ear disease and regularly assess hearing sensitivity with and without OM. In addition, the study of parental, linguistic, and socioeconomic factors are being considered in the analysis of results. Finally, samples of children from the general population including one large cohort study2l currently underway should provide data that will be applicable to the general paediatric population.
Our current view on OM is more global than in previous years. Now, rather than considering all children who have OM histories as at risk for sequelae, the recent view is that certain children or groups of children may be more susceptible to the effects of recurrent OM and mild hearing loss than others. Due to a particular combination of factors, some children may be more resilient and demonstrate little effect of OM. Such children ultimately experience better outcomes than do their peers with similar OM histories, but who may have very different background circumstances and experiences. Thus, increased or reduced vulnerability to specific developmental sequelae resulting from a history of OM may be mediated or moderated by one or more variables.22,23
For example, the timing, persistence, and degree of the hearing loss associated with middle-ear effusion appears to be an important mediator of outcome.2425 Early linguistic experiences (parents' language use and interactions with the child) also appear to exert a strong influence on young children's language development. Enriched language experiences may actually serve to overcome any negative effects of the hearing loss associated with OM.2223 Longitudinal studies have shown that a history of OM may be manifested differently at various stages of development. In our own studies' 24 26 of children from infancy through school age, we have found an apparent 'resolution' of early language delays by the time children entered school. However, academic problems emerged for some of the children when they encountered the challenges of a mainstream academic environment. Other investigators who have shown no effect of OM on early language development have reported that at school age, children may exhibit problems in the classroom828 and specific difficulties in certain cognitive domains.29 Thus, it is now clear that a complete view of OM and development necessitates the use of prospective research designs and longitudinal follow-up with analyses of all potential mediators and moderators of outcome.
Hearing Loss and Auditory Abilities
Before addressing recent views of language, speech, and educational outcomes, it is important to consider what is currently known about the hearing loss and other auditory sequelae of persistent OM in early childhood. The characteristics of the hearing loss associated with OME are different from permanent conductive or cochlear impairments in that the loss is temporary, variable in degree and duration, often recurrent, and sometimes asymmetric.l43-32 In theory, the variability of the input signal resulting from these hearing-loss characteristics make learning the auditory-linguistic code challenging for some children.7,8 ll 28,33-36
Peripheral sensitivity is obviously an important aspect of the study of OM. Furthermore, other auditory abilities, in addition to sensitivity, can be affected by OM. For example, listening with two ears allows individuals to more efficiently understand speech in noise, to localize sound accurately, and to easily perceive the first of multiple sounds arriving at the ears (precedence effect). Unilateral OM has been demonstrated to impair young infants' accurate orientation to sounds presented in the horizontal median plane.37 Recent studies show that older children with OM histories are less accurate in their localization abilities than are peers without such histories.5 The masking level difference (MLD) is a derived index that can be used to examine binaural auditory processing: the capacity of the auditory system (brainstem level) to detect subtle time and intensity differences between signals presented to both ears. Several research groups have found that children with OM histories had smaller MLDs compared to otitis-free children of the same age.'
Persistent conductive impairments during early childhood may also result in atypical findings on electrophysiologic indices of auditory brainstem pathway integrity. Several studies have reported atypical auditory brainstem response (ABR) findings in children with OM histories. These include prolonged absolute latencies of ABR waves III and V, prolonged I-III, III-V, and I-V interpeak latencies, and interaural interpeak-latency asymmetries.3-4' Thus far, only the study by Gunnarson and Finitzo4 documented OM and hearing prospectively through 18 months of age, and later found atypical ABR indices in children evaluated at 5 to 7 years of age. These researchers also derived the binaural interaction component (BIC) of the ABR, an index of binaural processing. They found that as a group, children with persistent early OM and hearing loss histories demonstrated the BIC less frequently than did children with infrequent or no early OM experience. Hall and Grose`" examined both the MLD and the ABR in children with and without OM histories and found a significant negative relationship between the MLD and ABR interaural interpeaklatency asymmetries (the greater the interaural asymmetry the smaller the MLD).
Collectively, these studies offer compelling evidence of atypical auditory indices, particularly binaural, as potential sequelae of early OM. These studies support the idea that OM in early life may be a form of `auditory deprivation.' It is cautioned, however, that the functional consequences of such atypical electrophysiologic and psychoacoustic findings remain to be determined.42 Some investigators suggest that children who have difficulties on complex listening tasks have a `central auditory processing disorder' (CAPD); indeed, some believe that early OM can cause CAPD.446 The majority of the studies linking OM to CAPD can again be criticized for flawed methodology2,15 and a failure to differentiate language impairments from primary auditory processing deficits.4749 Consider that if CAPD were a dysfunction specific to the processing of auditory information, then it would be reasonable to expect auditory electrophysiologic and psychoacoustic evidence of such a deficit. To date, this auditory-specific evidence has not been demonstrated in children labelled CAPD and, in particular, in those who also have histories of oM.49 Thus, any relationship between OM and CAPD remains to be fully delineated.
Important questions remain regarding hearing loss and OM. Such questions include whether or not children who have greater hearing loss for protracted periods of time have more significant developmental sequelae than do those with lesser involvement. In addition, it remains to be determined which periods (months or years) of life are most sensitive with regard to any negative effects of hearing loss. Thus, little is currently known about the relationship between degree, configuration, and duration of hearing loss and any communication and educational consequences. Language and Speech Development
While specific questions remain, the overall importance of early auditory experience in the development of spoken language is well recognized. Studies completed by developmental psychologists have clearly established that infants who hear normally accurately discriminate the sounds of spoken language essentially at birth.so Within several months after birth, infants distinguish the speech sounds of their native language from those of a foreign dialect.sl Abundant auditory-linguistic experiences in the first year of life serve as the foundation for later expressive language abilities. The effects of congenital permanent hearing loss of moderate-toprofound degree on oral/aural language development in early life are well established.525) However, less is known about the specific consequences of milder forms of permanent congenital hearing loss (< 40-dB HL, unilateral losses, or sloping hearing impairments) on communication acquisition. Only recently are the effects of the temporary, fluctuant, mild conductive hearing loss associated with OM on language and speech development beginning to receive attention.
Several prospective studies have found that recurrent OM in the first and second years of life negatively influence global receptive and expressive language abilities when children were assessed at preschool and/or at school ages.'Z.zs,25,54,ss However, some researchers who looked at both receptive and expressive language failed to find differences in receptive language abilities between children with and without OM histories, while expressive language deficits were evident,24,2656 or the converse.57 Still other prospective investigations of language failed to demonstrate differences on global, standardized measures of either receptive or expressive language abilities.58,59 Other prospective studies found significant effects of OM on aspects of language such as phonology,6,61 syntax,60 semantics,ss and pragmatics.Ra,22
It is clear that using only standardized measures of global language ability may fail to reveal subtle but potentially important differences in the development of expressive and receptive language skills in infants and young children with OM histories. Recent studies that have completed in-depth analyses on one or more of these specific language abilities have found delays or differences in production of speech phonemes in young children with OM histories compared to OM-free peers.606263 Petinou et al.64 found that children with mild hearing loss (> 20-dB HL PTA) associated with early OM made more phonologic and morphologic perceptual errors at 22 to 24 months of age than did peers with normal hearing in the first 2 years of life. When assessed at school age, both speech-sound discrimination and identification appears to be negatively influenced by a history of OM.48'65'66 One recent study48 that used a factorial design found that children who had both a diagnosed language disorder and a history of OM had the poorest results on a speech-perception task. Such auditory-perceptual problems may adversely affect prereading27 and reading abilities,60,67,68 skills that are based on a previously established representation of the phonologic code of aural language.69,70
In their review of the results of 15 studies that used a prospective research design and careful documentation of OM, Roberts and Wallacel6 concluded that there now is sufficient empiric evidence to suggest that expressive language and pragmatics (language use) are negatively influenced by a history of OM.
Educational Performance Cognitive Abilities
Wallace and Hooper's recent review"8 of the results of 12 prospective studies of OM and cognition revealed a somewhat different view than had been suggested by the earlier retrospective investigations (see above). They characterized the findings of the vast majority of prospective studies as "essentially negative." In other words, regardless of the age range studied (infancy, preschool, or school-age), the majority of prospective studies failed to show a relationship between measured cognitive abilities and early OM status. The two prospective studies that did report significant findings had modest correlations,6 or a one-time significant result that was not replicated when the same children were studied at older ages.S7 The study of Roberts and her colleagues71 that examined hearing prospectively, as well as OM history, found associations between neither factor and cognitive abilities. Thus, the Wallace and Hooper"8 review concluded that early OM is not related to later intellectual functioning. Their caution was that their conclusion was based on studies that used global measures of cognitive ability. Thus, more specific attributes of intelligence such as attention, memory, and verbal reasoning could be differentially affected by histories of OM and hearing loss.
Academic Abilities
Of the eight cohorts of children who were the subjects of recent prospective investigations, Wallace and Hooper'8 found five research teams that reported a significant relationship between early OM and later academic performance. However, while prospective, not all research groups documented OM beginning at the same point in childhood. Three research teams studied children's middle-ear status beginning in early infancy.927-29,60,71 Two of these groups found an association between lower academic achievement scores on reading,27,60 mathematics,6 and in teachers' perceptions of educational risk27 and a history of OM. Studies of the third cohort reported no academic difficulties in OM-positive and OM-free children when studied at kindergarten, elementary, and middle-school age.9,zs,29,71 Of the five remaining prospective studies, OM was documented beginning either at preschool68 or at school age.67 Overall, these prospective studies found spelling,6' writing,68 and reading67,72 difficulties in children who had OM histories (by otoscopic inspection), or more than one abnormal tympanogram during the study period, than in children without such positive findings.
Difficulty maintaining attention, as well as behaviour problems in the classroom, have also been raised as potential sequelae of OM. In the academic setting, these issues are particularly important, because they profoundly affect the child's potential for academic success. Prospective studies that used direct observations, specific measures, as well as teacher and parent rating scales have been used to study these domains. Preschoolers and school-aged children have been studied, some cohorts at more than one age. Feagans and her colleagues73 found preschoolers' ability to maintain their attention in day care to be related to their early OM history: the more time with OM, the less time spent attending. Other studies of both preschool and school-age children have reported mixed results with regard to behaviour and attention and OM. In some studies, a relationship between early OM history and teacher ratings of task orientation, independence, and behaviour was found.9,27,Zs,72 Other studies using similar rating scales and a direct measure of attention (a continuous performance task) did not find associations between attention and behaviour and OM.71,74
Higher order (cortical) auditory abilities, such as auditory tasks that require children to selectively listen (attend) to one message and ignore another, have been found to be negatively influenced by an early history of OM..11--13 In one of our studies,ll we found differences in the selective listening abilities of 4 year olds with and without OM. Performance at 4 years was later related to teachers' ratings of academic performance and to class participation at 6 years of age,27 but not to their ratings of behaviour or attention in the classroom.
Wallace and Hooper"8 concluded that the results of prospective studies of academic abilities suggest that a history of OM has the strongest influence on skills that are linguistically based. These include reading, spelling, and written language, rather than mathematical skills. They also concluded that there is some literature support for a relationship between OM and attention, hyperactivity, and the diagnosis of attention-deficit hyperactivity disorder (ADHD).ls However, important factors (parents' educational level, quality of the home and school environment, age of OM onset and resolution, OM and hearing loss persisting into the school years, and acoustic demands of the classroom) that could affect academic skills, attention, and behaviour sometimes were not considered.
Conclusions
By the year 2000, our understanding of children with histories of OM in early life will be considered well advanced over the body of knowledge that was available 30 years ago. However, more prospective research on otitis media and development will be needed to gain further insight into the risk indicators for long-term sequelae in the individual child. Careful documentation of OM and any associated hearing loss will remain crucial to our full appreciation of the consequences of middle-ear disease. In addition, the role of other mediating and moderating variables that can affect language of children with OM histories will require further exploration. Information obtained from future studies of OM should provide answers to fundamental questions regarding critical or sensitive periods in humans, minimal auditory deprivation, and the ontogeny of language and speech. The studies required for addressing the issues reviewed here are long term, difficult to control, and expensive. However, it is only through welldesigned and well-executed studies of language, speech, and educational outcomes that physicians, communication specialists, and educators will have the requisite knowledge to better serve children with OM and their families in the new millennium.
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Judith S. Gravel and Ina F. Wallace: Albert Einstein College of Medicine, Bronx, New York; Ina F. Wallace: Research Triangle Institute, Research Triangle, North Carolina. Supported by Research Grant 5 P50 DC 00223 from the National Institute on Deafness and Other Communication Disorders, National Institutes of Health. Address reprint requests to: Dr. Judith S. Gravel, Rose F. Kennedy Center, Room 843, Albert Einstein College of Medicine, 1300 Morris Park Avenue, Bronx, NY 10461.
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