The Cleft Palate–Craniofacial Journal 53(2) pp. 147–156 March 2016 Ó Copyright 2016 American Cleft Palate–Craniofacial Association

ORIGINAL ARTICLE Behavioral Signs of (Central) Auditory Processing Disorder in Children With Nonsyndromic Cleft Lip and/or Palate: A Parental Questionnaire Approach Xiaoran Ma, Ph.D., Bradley McPherson, Ph.D., Lian Ma, Ph.D., M.D. Objective: Children with nonsyndromic cleft lip and/or palate often have a high prevalence of middle ear dysfunction. However, there are also indications that they may have a higher prevalence of (central) auditory processing disorder. This study used Fisher’s Auditory Problems Checklist for caregivers to determine whether children with nonsyndromic cleft lip and/or palate have potentially more auditory processing difficulties compared with craniofacially normal children. Methods: Caregivers of 147 school-aged children with nonsyndromic cleft lip and/or palate were recruited for the study. This group was divided into three subgroups: cleft lip, cleft palate, and cleft lip and palate. Caregivers of 60 craniofacially normal children were recruited as a control group. Hearing health tests were conducted to evaluate peripheral hearing. Caregivers of children who passed this assessment battery completed Fisher’s Auditory Problems Checklist, which contains 25 questions related to behaviors linked to (central) auditory processing disorder. Results: Children with cleft palate showed the lowest scores on the Fisher’s Auditory Problems Checklist questionnaire, consistent with a higher index of suspicion for (central) auditory processing disorder. There was a significant difference in the manifestation of (central) auditory processing disorder–linked behaviors between the cleft palate and the control groups. The most common behaviors reported in the nonsyndromic cleft lip and/or palate group were short attention span and reduced learning motivation, along with hearing difficulties in noise. Conclusion: A higher occurrence of (central) auditory processing disorder–linked behaviors were found in children with nonsyndromic cleft lip and/or palate, particularly cleft palate. Auditory processing abilities should not be ignored in children with nonsyndromic cleft lip and/ or palate, and it is necessary to consider assessment tests for (central) auditory processing disorder when an auditory diagnosis is made for this population. KEY WORDS:

auditory processing disorder, cleft lip and/or palate, hearing loss, questionnaire

Clefts of the lip and/or palate (CL/P) are common congenital craniofacial deformities, appearing as human birth defects worldwide. A recent research study (International Perinatal Database of Typical Oral Clefts, 2011) indicated the overall prevalence of CL/P was 0.992 per 1000 live births, and the prevalence of cleft lip and palate was significantly greater than cleft lip only. Among patients with cleft disorders, the majority (70%) are regarded as nonsyndromic cleft lip and/or palate (NSCL/P) cases, which refers to a cleft not associated with other anomalies (Stanier and Moore, 2004). The current incidence of CL/P

in China is also of great concern. Every year there are at least 30,000 babies with CL/P born in China (Wang et al., 2009).The prevalence rate of all types of cleft is 1.3 per 1000 in China, with 1.2 per 1000 being nonsyndromic CL/P (Cooper et al., 2006). Regarding hearing problems in the population with nonsyndromic cleft lip and/or palate (NSCL/P), considerable emphasis has been given to middle ear deficits that are most likely due to eustachian tube dysfunction (Bluestone and Doyle, 1988; Huang et al., 1997; Kemker and Antonelli, 2004; Sheer et al., 2010). Jarvis (1976) indicated that the percentage of middle ear problems was more than 60% in a study of 350 children with cleft palate. More recently, Flynn and colleagues (2009) found that the prevalence of otitis media with effusion in children with unilateral cleft lip and palate (74.7%) was significantly higher than for children without clefts (19.4%). Conductive hearing loss in children with NSCL/P is typically bilateral, fluctuating, and in the mild to moderate range (Yang and McPherson, 2007). Even mild conductive hearing loss can lead not only to communication problems but also to

Dr. X. Ma is doctoral student and Dr. McPherson is Professor, Division of Speech and Hearing Sciences, The University of Hong Kong, Hong Kong. Dr. L. Ma is Professor, Cleft Lip and Palate Center, Peking University School of Stomatology, Beijing, China. Submitted February 2014; Revised June 2014, September 2014; Accepted October 2014. Address correspondence to: Xiaoran Ma, Division of Speech and HearingSciences,The University ofHongKong,7F, MengWah Complex, Pokfulam Road, Hong Kong. E-mail [email protected]. DOI: 10.1597/14-057 147

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learning disorders, language disorders, and speech disorders if timely treatment is not obtained (Kuo et al., 2013). These disorders will often have a negative effect on psychological health and limit the social development of children (Kemker and Antonelli, 2004) and family quality of life in general (Brouwer et al., 2005). Inner ear dysfunction is rare in children with NSCL/P compared with children with syndromic clefts (Yang and McPherson, 2007). However, little is known concerning the prevalence of (central) auditory processing disorder, or (C)APD, in this population. (Central) auditory processing disorder is defined as a hearing deficit resulting from impaired brain function, characterized by problems with cognition and discrimination of auditory signals that do not arise from higher order cognitive and/or language related functions (British Society of Audiology, 2005). According to a report of American Speech-Language-Hearing Association (ASHA, 1997), patients with (C)APD typically show difficulties or poor performance in one or more of the following behaviors: sound localization and lateralization; auditory discrimination; auditory pattern recognition; temporal aspects of audition. In addition, patients typically show auditory performance decrements with competing acoustic signals and degraded acoustic signals. Evidence indicates that differences exist in auditory brain structure between patients with NSCL/P and their craniofacially normal peers. A series of studies on young adult men with isolated cleft of the lip, palate, or both by Nopoulos and colleagues (2000, 2002, 2006) revealed that patients with orofacial clefts had radiologically abnormal cortical regions, with the most significant differences in the left temporal lobe—the location of the auditory cortical area—which may lead to differences in auditory processing abilities. In addition, significantly decreased volume and thickness of the left superior temporal plane and other cortical developmental abnormalities have been found in 6to 24-month-old infants with CL/P (Yang et al., 2012b). Auditory evoked potentials also have been used to assess auditory processing difficulties in infants and children with NSCL/P. Smaller amplitudes of P150 and the N250 responses to tones have been found in children with other craniofacial malformations, such as plagiocephaly, which suggested central auditory processing deficits may exist in this general population (Balan et al., 2002). Cheour et al. (1998, 1999) used mismatch negativity potential (MMN) measures to assess infants and school-aged children with oral clefts compared with craniofacially normal controls and found abnormal MMN amplitude and significantly shorter auditory sensory memory in the CL/P group, which is consistent with more recent findings for infants with NSCL/P (Yang et al., 2012a). In view of the physiological potential for (C)APD behaviors in children with NSCL/P, this study aimed to analyze information provided by caregivers, who were mainly parents, to determine whether a higher prevalence of

typical (C)APD-linked behaviors were observed in this group compared with craniofacially normal children by using Fisher’s Auditory Problems Checklist (FAPC; Fisher, 1976). In a comprehensive test battery for (C)APD, questionnaires have been recommended as important screening tools prior to formal diagnosis because they can reduce the time and resources lost by inappropriate referrals (Keith, 2000; Bellis, 2003; Schow and Seikel, 2007). A screening procedure for (C)APD may also accelerate correct diagnosis and management for suspected children (Musiek et al., 1990). Although there are no universally accepted ideal screening procedures for (C)APD, some auditory questionnaires and checklists have been commonly applied for screening (Emanuel, 2002). In a survey concerning auditory processing assessment practices in the United States, Emanuel (2002) reported that the most popular questionnaires were the Children’s Auditory Performance Scale (Smoski et al., 1998), the FAPC (Fisher, 1976), and the Screening Identification for Targeting Educational Risk (Anderson, 1989). As Wilson et al. (2011) summarized, the benefits of using these types of questionnaires include ease of administration, low cost, and the ability to systematically obtain a comprehensive history and developmental information. On the other hand, the most obvious disadvantages are the potential subjectivity and biases of the person answering the checklist. In addition, some researchers (Jerger & Musiek, 2000) also suggested that (C)APD questionnaires were primarily designed to maximize sensitivity, which usually implies a lack of test specificity. In this respect, questionnaires are not recommended as a diagnostic tool for accurate (C)APD assessment. Despite these drawbacks, as a means to highlight concerns from parents and alert clinicians to suspect behaviors, as well as to encourage earlier intervention for (C)APD, screening by questionnaire has advantages. In this study, a Chinese version of FAPC was used. Fisher’s Auditory Problems Checklist contains questions that directly address the ASHA criteria, such as those involving discrimination ability and degraded processing in a noisy environment. Also, some attentional and memory issues are included that are not directly reflected in the ASHA criteria (Schow and Seikel, 2007).This checklist was selected because it gives a good overview of children’s functional listening behaviors in the classroom (Bellis, 2003c), and the questions concentrate on the risk of (C)APD rather than on other learning disabilities. Also, the checklist is designed to be completed by parents, and not solely by teachers, which made it appropriate for administration in the current study. METHODS Participants Caregivers of 147 children with NSCL/P (98 boys and 49 girls) aged 6.00 to 15.67 years (mean, 10.06 years)

Ma et al., AUDITORY BEHAVIORS IN CHILDREN WITH CLEFT LIP/PALATE

were recruited into the current study. Among them there were 86 mothers, 54 fathers, one aunt, one older sibling, and two grandmothers. Also, three participants were guardians of children who were orphans. All the participants were very familiar with the daily routine and educational performance of their child. All of the children were native Mandarin speakers and attended regular schools. They were divided into three subgroups by cleft type: 37 children with isolated cleft lip (CL), 27 children with isolated cleft palate (CP), and 83 children with combined cleft lip and palate (CLP). The latter subgroup was further classified as unilateral CLP or bilateral CLP. A purposive sampling method was used to collect data for both the NSCL/P and control groups. The children and adolescents were visiting the outpatient department of the Cleft Lip and Palate Clinic Center, Beijing Stomatology Hospital, for further consultation, as recommended by their primary care doctors, at the time of data collection. The hospital is a large polyclinic and patients visit the Center from all regions of China. The children were from 22 provinces and municipalities in China, with more than one third of them from Beijing and neighboring Hebei province. The control group comprised 60 participants including 17 fathers, 38 mothers, two grandmothers, and three relatives of craniofacially normal children (25 boys and 35 girls) aged 6.00 to 15.50 years (mean, 10.16 years). Some of the craniofacially normal children were the children of the doctors and nurses in Beijing Stomatology Hospital, and others were these children’s school classmates who lived nearby. In addition, some normal children were recruited from the family members who accompanied their brothers or sisters to see doctors in this hospital. Data collection was conducted during the summer and winter school holiday periods of Chinese regular schools from July to August 2012, February to March 2013, and July to September 2013. Informed consent was obtained before participation in the research program, and parent consent and student assent forms were completed. The study was approved by the Human Research Ethics Committee for Nonclinical Faculties, The University of Hong Kong (reference number EA140811). Materials The FAPC questionnaire contains 25 questions referring to typical behavioral problems noted in children with (C)APD (Fisher, 1976). The Chinese version used in the present study was completed following bilingual translation work. The steps in the translation process adhered to guidelines for crosscultural questionnaire adaptation (Guillemin et al., 1993), which recommended preserving the meaning of the questionnaire in a Chinese cultural setting. The procedure involved translations and back-translations

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by qualified individuals. First, the original English version of the checklist was translated into a draft Chinese version by the first author. Second, this draft was translated back from Chinese into English by two native Chinese speakers. These two back-translators were educated bilingual individuals who were fluent in the idioms and colloquial forms of English. The aim of this work was to locate in the initial translation divergent items and phrases with potential for ambiguity and to revise the draft version accordingly. After revising some words and phrases in the Chineselanguage version, back-translations were trialed a second time and found to be appropriate. The scoring approach was the same as in the original Englishlanguage version. Procedure All participant children with NSCL/P and their normal peers undertook auditory screening tests to assess their peripheral hearing. The screening protocol followed ASHA (1997) guidelines for screening hearing impairment and middle ear disorders and included otoscopic examination, pure-tone audiometry, 226-Hz probe tone tympanometry, and ipsilateral 1-kHz acoustic reflex threshold measures. A diagnostic otoscope, an SA 204 diagnostic audiometer (Entomed, Malmo, Sweden), and a GSI 39 automatic tympanometry middle ear analyzer (GSI Corp., Eden Prairie, MN) were used to perform the assessment. Screening tests were conducted in a quiet research room, and the background noise was no more than 35 dBA at any time. To be considered to have normal hearing, the external ear canal was visibly unobstructed, with any cerumen impaction removed before testing was attempted. Each participant child’s pure-tone audiometric air-conduction threshold level was required to be 25 dB HL or less on the average for four frequencies (0.5, 1, 2, and 4 kHz) in both ears. These pure tones are considered to reflect the main speech-related frequencies in real life (World Health Organization, 1991). Furthermore, all recruited children were required to have type A tympanograms, which are characterized by a clear peak maximum at or near 0 daPa, with negative middle ear pressure not equal to or less than 100 daPa (Jerger, 1970). Normal acoustic reflex thresholds range from 85 to 100 dB SPL (Gelfand, 2009), and participant children were considered to have normal reflex function if thresholds were 100 dB SPL at 1 kHz. If a child met the screening criteria for bilateral normal peripheral auditory function, the caregiver then completed the FAPC. The caregiver accompanying the child checked the items that corresponded best to the situation of their child. The final questionnaire score is presented as a percentage. For each numbered item not checked, 4% credit is given; for example, if only one item is considered to be a

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concern by the observer, the score is 4% 3 (25  1) ¼ 96%. According to the questionnaire developer, a result of less than 72% (i.e., more than seven items are checked) indicates that a child may be at risk for (C)APD (Fisher, 1976). In the process of completing the questionnaire, participants were encouraged to raise questions if they were not clear about questionnaire items. On infrequent occasions, for instance, when the score was very low or the participant remained on one item for a long time, the first author communicated with the participants to clarify potential misunderstandings. Also, if caregivers were not familiar with their child’s performance on some items mentioned, they were advised to contact other persons familiar with the child who could provide information. Caregivers were also asked to complete a case history providing details of family and social situation, child’s education background, mother’s prenatal history, and birth conditions, as well as some general developmental information derived from parental observations, including their impression of the hearing ability and speech/ language development of their child. Children with language or cognitive problems were not recruited in the current study. Statistical Analysis Descriptive statistics were calculated, based on numbers and percentages of FAPC scores for children with NSCL/P according to cleft subgroups and also on outcomes for control group children, including range and averages. A chi-square test was used as an inferential statistical approach to compare differences between the combined NSCL/P and the control groups as well as differences among NSCL/P cleft subgroups. A P value ,.05 was considered statistically significant. RESULTS In the current study, there were 184 children with NSCL/ P willing to participate in the research project and who undertook the hearing health tests. Based on the exclusion criteria, 37 children (20.1%) had mild to moderate conductive hearing loss, presenting with type B/C tympanograms, absent acoustic reflex thresholds, and/or more than 25 dB HL hearing thresholds at the average for four frequencies (0.5, 1, 2, and 4 kHz) in one or both ears. The majority of these excluded children had bilateral hearing loss, and only three had unilateral hearing loss. Caregivers of children with middle ear problems did not complete FAPC. Therefore, caregivers of 147 children with NSCL/P participated in the study. Prior to hearing health tests, the external ear canal of each child was visibly unobstructed, with any cerumen impaction removed. All of children had type A tympanograms. For ipsilateral 1-kHz acoustic reflex thresholds, left

and right ears of children with NSCL/P were 103.15 6 4.24 dB HL and 102.67 6 4.70 dB HL, respectively, and for the control group they were 102.29 6 5.20 dB HL and 101.78 6 5.39 dB HL, respectively. Pure-tone test results for children with NSCL/P indicated that the means and standard deviations of the four-frequency average threshold (500 Hz, 1 kHz, 2 kHz, and 4 kHz) were 9.70 6 4.87 dB HL and 9.97 6 4.72 dB HL for left and right ears, respectively. For the control group, means and standard deviations were 8.33 6 3.12 dB HL and 8.29 6 3.98 dB HL for left and right ears, respectively. Two-way analysis of variance showed there was no significant ear effect on puretone test results for both children with NSCL/P and control group children. However, the four-frequency average threshold of the NSCL/P group was significantly higher than that of the control group (F1.401 ¼ 5.05, P , .05), although there was no significant difference of acoustic reflex thresholds between these two groups. Figure 1 shows the pure–tone test thresholds of each tested frequency in children with NSCL/P. According to the different types of clefting noted in the participant children, three subgroups of children with cleft and a control group were formed for analysis: (1) CL group—children with isolated cleft lip; (2) CP group— children with isolated cleft palate, including submucous cleft palate; (3) CLP group—children with combined cleft lip and palate, include unilateral CLP and bilateral CLP; (4) Control group—craniofacially normal children. Table 1 shows a summary in terms of minimum, maximum, and average questionnaire percentage scores for each cleft subgroup and the control group. Children with CP showed the lowest average caregiver score (84%), followed by the bilateral CLP group (86%) and the combined CLP group (89%). Children with CL had the best FAPC performance (95%), which was identical to that noted for their craniofacially normal peers. A chi-square test was used to compare the differences in proportions of at-risk occurrence for (C)APD conditions between NSCL/P and control groups, with at-risk status being defined by FAPC’s standard criterion ,72% score (Fisher, 1976). The difference between the combined NSCL/P group and the control group was not significant. However, there was a significant difference between the CL subgroup and the CP subgroup (v21 ¼ 7.43, P , .05). Also, manifestation of (C)APD-linked behaviors in the CP subgroup was significantly different from the control group, (v21 ¼ 8.24, P , .05). On the basis of the calculated odds ratio, the odds of children with CP failing FAPC were 13.9 times higher than craniofacially normal children. Among the 25 items of FAPC, item 21: Has an articulation (phonology) problem; item 7: Has a short attention span; and item 23: Lacks motivation to learn were the most common problems noted in children with clefting disorders. Because a craniofacial malformation exists in children with CP and children with CLP, an articulation deficit is often found in this population regardless of their auditory

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FIGURE 1

151

Means and standard deviations of pure-tone test thresholds of each tested frequency in children with NSCL/P.

abilities (Albery and Grunwell, 1993). Therefore, results were reanalyzed after item 21 was excluded. Figure 2 shows the distribution of the most common 10 items noted by parents with item 21 excluded. Similar to the results presented in the previous paragraph, there was no significant difference between the combined NSCL/P group and the control group. However, when analyzed according to type of clefting, a significant difference was found between the CP group and the control group, (v21 ¼ 5.94, P , .05). Figure 3 shows the most common 10 items in each cleft type group and the control group, with item 21 excluded. The most common problems noted for each group were (1) CL group—item 23: Lacks motivation to learn (21.6%); (2) CP group—item 7: Has a short attention span (40.7%); (3) CLP group—item 7: Has a short attention span (27.7%); (4) Control group—item 2: Has a history of ear infection(s) (13.3%). Because the primary task for auditory processing evaluation tools is distinguishing patients with (C)APD from the normal population, the pass/fail criteria are usually established on the basis of normative data. In order to balance test sensitivity and specificity well to obtain appropriate combined test efficiency, cutoff scores for (C)APD tests are generally set as two standard deviations below the mean (Bellis, 2003b; American Academy of Audiology, 2010a). Following original FAPC criterion, the cutoff score was 72%, which may not adequately distinguish children having negative results from the other participants using the current Chinese translation of the questionnaire. Figure 4 illustrates the frequencies of FAPC results appearing in both NSCL/P and control groups. In order to further find relationships between cleft types in children with NSCL/P and to make potential comparisons more accurate, an alternative cutoff score was established using the mean of the control group minus two standard

deviations. Consequently, the new cutoff score was (0.96  0.07332)3100%¼81%. Table 2 shows the distribution of occurrence of the manifestation of (C)APD-linked behaviors with this alternative cutoff score. A chi-square test showed that, without consideration of articulation problems and using ,81% as the cutoff score, there was a significant difference between the CL and CP groups (v21 ¼ 6.52, P , .05). On the basis of the odds ratio, the odds of children with CP failing FAPC were 5.6 times higher than for children with CL. Also, manifestation of (C)APD-linked behaviors in the CP group was significantly different from those in the control group (v21 ¼ 10.42, P , .05). On the basis of the odds ratio, the odds of children with CP failing FAPC were 1.9 times higher than for craniofacially normal children. DISCUSSION In the current study, before caregivers completed the FAPC, all participant children undertook a series of screening tests for peripheral hearing, including otoscopic examination, pure-tone audiometry, 226-Hz probe tone TABLE 1

FAPC Descriptive Statistics According to Cleft Type*

Groups

Min (%)

Max (%)

Average (%)

n

NSCL/P CL CP Unilateral CLP Bilateral CLP CLP Control

80 32 44 56 44 60

100 100 100 100 100 100

95 84 91 86 89 95

37 27 55 28 83 60

Children scoring ,72%, n (%)

0 5 3 2 5 1

(0) (18.5) (5.5) (7.1) (6.0) (1.7)

* FAPC ¼ Fisher’s Auditory Problems Checklist; Min ¼ minimum; Max ¼ maximum; NSCL/P ¼ nonsyndromic cleft lip and/or palate; CL ¼ cleft lip; CP ¼ cleft palate; CLP ¼ cleft lip and palate.

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FIGURE 2 Distribution of the most common 10 FAPC items in the NSCL/P group compared with control group participant results, without consideration of articulation (phonology) problems.

FIGURE 3 Distribution of the most common 10 FAPC items in cleft disorder subgroups compared with control group participant results, excluding articulation problems.

Ma et al., AUDITORY BEHAVIORS IN CHILDREN WITH CLEFT LIP/PALATE

FIGURE 4

Frequencies of FAPC results for both NSCL/P and control groups.

tympanometry, and ipsilateral 1-kHz acoustic reflex threshold measures, as well as a basic medical history to exclude those with genetic or other syndromic disorders. Parents of the children who met all the criteria, which indicated the children had normal peripheral hearing status, completed the FAPC questionnaire. Although testing indicated that children with NSCL/P had significantly higher pure-tone thresholds than the craniofacially normal children, the results were still within the normal range— which was less than 25 dB HL— and the four-frequency average thresholds for 95% of children with cleft disorders were less than 20 dB HL. The reason for completing routine auditory tests is that the eustachian tube of individuals with CL/P is often bent in a caudal direction, which creates an obstacle to the ventilation function (Broder et al., 1998), and this often leads to otitis media with effusion and hearing loss. Although improvement of hearing status is usually shown in children with CL/P with increasing age, a significant proportion of this group may have delayed recovery from otitis media (Yang et al., 2007). It has been suggested that even mild hearing loss in children with chronic otitis media may lead to greater problems in speech and language acquisition, cognitive development, and social maturation compared with otologically normal children (Kemker and Antonelli, 2004). Consequently, in order to attempt to eliminate a potential additional negative effect on questionnaire results, children with abnormal peripheral hearing at the time of assessment were not recruited in the study. According to the results obtained, 24 participants reported that their children with NSCL/P had a prior history of ear infection, accounting for 16.3% of the NSCL/P group. However, only two of caregivers (2.4%) TABLE 2

indicated that previous middle ear dysfunction affected their child’s hearing sensitivity. In the control group, eight parents (13.3%) marked their children as previously having ear infections. The minor and relatively matched percentage of previous known peripheral hearing loss in both NSCL/P and control groups suggests this should not be an important confounding factor in the current study. According to the results obtained, the most typical problem occurring in children with CP and children with CLP is an articulation deficit, with 62.9% and 48.2%, respectively, of respondents mentioning this issue. This phenomenon was rarely noted in children with CP, and only 5.4% of this group was noted to have the problem. Children with CP typically show disordered speech characteristics such as hypernasality, hyponasality, audible nasal air emission and/or nasal turbulence, consonant production errors, and voice disorder (Henningsson et al., 2008). In this study the focus was on the auditory processing abilities in children with NSCL/P, and to exclude the impact of associated articulation problems in children with CP, item 21: Has an articulation (phonology) problem was excluded from much of the analysis. Of the remaining 24 items on the questionnaire, item 7: Has a short attention span and item 23: Lacks motivation to learn were the problems most typically found in parental reports for all of CL, CP, and CLP group children. Poor auditory attention and susceptibility to distraction by auditory stimuli are typical behaviors in children with (C)APD (American Academy of Audiology, 2014), and related symptoms include having difficulties hearing in background noise, becoming easily fatigued, and needing information to be repeated. Attention problems are also

Distribution of Occurrence of (C)APD-Linked Behaviors in Children for NSCL/P and Control Groups (Cutoff Score Is ,81%)*

Manifestation of (C)APD Present Absent Total

153

CL Group, n (%)

CP Group, n (%)

CLP Group, n (%)

Total, n (With Cleft)

Control Group, n (%)

3 (8.1) 34 (91.9) 37 (100)

9 (33.3) 18 (66.7) 27 (100)

17 (20.5) 66 (79.5) 83 (100)

29 (19.7) 118 (80.3) 147 (100)

4 (6.7) 56 (93.3) 60 (100)

* (C)APD ¼ (central) auditory processing disorder; NSCL/P ¼ nonsyndromic cleft lip and/or palate; CL ¼ cleft lip; CP ¼ cleft palate; CLP ¼ cleft lip and palate.

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associated with another cognitive disorder—attention deficit hyperactivity disorder (ADHD)—that has considerable behavioral overlap with (C)APD. However, the behaviors do not share the same sources. Cognitive disorders including disorganization and executive dysfunction are thought to be responsible for ADHD inattentiveness; whereas, children with (C)APD have difficulties with auditory input, and processing information through the auditory modality is not optimal (Geffner, 2013). Negative performance on auditory attention tasks in children with cleft disorders was also found in a Brazilian study (Minardi et al., 2004). This also used FAPC as an assessment tool and noted the abilities of hearing discrimination, hearing attention, and language and speech problems in noise as the most common problems found in children with CL/P. In contrast to the present study, the subgroups in the Brazilian research included children with cleft and hearing loss, children with cleft and no hearing loss, and a control group of children without cleft and hearing loss. They found that all of children with cleft showed (C)APD-linked behaviors, regardless of hearing status. In the current study, children with current hearing loss were not recruited due to the potential negative effect of current hearing loss on the FAPC scores. The most apparent problem in children with CL/P and no hearing loss in the Brazilian study was a deficit in auditory discrimination rather than in auditory attention as in the current study. However, possible differences of auditory processing abilities among cleft types were not considered in the former study. In addition to auditory attention, lack of motivation to learn was also an important issue in the current study. One third of all participants with NSCL/P, including 26.5% for CLP group and 21.6% for CL group, thought their children had this problem. This is consistent with other investigations that showed poorer academic performance by children with NSCL/P than by their normal peers. Broder et al. (1998) reported a study of 90 American children aged 6 to 18 years with NSCL/P, in which 46% had learning disability, 47% had deficient educational progress, and the grade retention rate for the group was 27%. More recently, a population-based register study (Persson et al., 2012) focused on the academic achievement and physical education of Swedish children with CL/P aged 16 years. The results indicated significant deficits in their performance, both in academic and physical skills outcomes, compared with craniofacially normal children. In addition to auditory attention and learning motivation, easy distraction by background sound and having difficulty with phonics were also prominent issues in children with NSCL/P in the current study. According to a report from ASHA (1997), children may be considered as having (C)APD if they have difficulties on auditory discrimination and/or hearing performance with competing acoustic signals. As a result, there appears to be a probability that children with orofacial clefts have more (C)APD-linked behaviors than their craniofacially normal peers.

According to the criterion set by the FAPC questionnaire developer, children scoring less than 72% may be at-risk for (C)APD. In order to distinguish children with poor performance who could be missed with the original wide criterion range of the English questionnaire, a stricter cutoff score was established by using a criterion of two standard deviations below the mean score. Consequently, the alternative criterion for children for both groups was 81%, and children with scores less than this cutoff value were considered to show (C)APD-linked behaviors. Analysis with the new pass/fail criterion was consistent with the initial analysis of cleft and control group FAPC results, given that scores for CP group were significantly lower than control group. Furthermore, significant differences were also found between CL and CP groups, indicating that children with CL have better performance than those in the CP group, also similar to what was found in the previous analysis with 72% as the cutoff score. This is a reasonable outcome because children with CL have no maxillofacial deficits of the soft and hard palates and may have less likelihood of cleft-associated cortical abnormalities. In addition, CL is almost never responsible for articulation dysfunction, and peripheral hearing problems appear less frequently in this population than in other cleft types (Peterson-Falzone et al., 2010). Furthermore, the current study results clearly indicated individuals with CP showed the most negative FAPC outcomes, followed by individuals with CLP, and children with CL showed the least risk for auditory processing disorders. This finding is consistent with Persson et al. (2012), who also found poorer academic performance in children with CP. Without consideration of articulation problems and when using 72% as the cutoff criterion, CP group scores were significantly lower than those of the control group. The relationship between hearing deficits and type of cleft has been repeatedly investigated (Drettner, 1960; Masters et al., 1960; Pannbacker, 1969; Handzic-Cuk ˇ et al., 2001; Sheahan et al., 2003). However, research has yielded inconsistent results. Although how prevalence of hearing loss, middle ear dysfunction, or other hearing problems relates to different type of cleft disorders is still unclear, it is worthwhile highlighting the need to consider cleft types in studies of auditory processing problems and educational achievement in this group of children. (Central) Auditory Processing Disorder may be associated with neurological disorders, delayed central nervous system development, or other developmental disorders such as dyslexia and language impairment (Bamiou et al., 2001). The results of the current study suggest that compared with craniofacially normal school age children, children with NSCL/P are more at risk for (C)APD, particularly children with CP. This may be for several main reasons. First, previous episodes of otitis media may affect auditory processing abilities. A higher prevalence of reported history of chronic otitis media with effusion was found in children

Ma et al., AUDITORY BEHAVIORS IN CHILDREN WITH CLEFT LIP/PALATE

with (C)APD than children without (C)APD (Dawes et al., 2008). Otitis media with effusion has been hypothesized to affect auditory processing skills due to its disruption of normal binaural hearing and possible consequent auditory system neural changes that may delay or halt normal central nervous system development (Roberts et al., 2004). As a result, an awareness of possible long-term sequelae of middle ear problems occurring in children with NSCL/P should be raised in both clinicians and parents. Early intervention to eliminate the hearing loss produced by middle ear dysfunction is important to avoid further effects on auditory processing abilities (Moore et al., 2003). Second, as mentioned earlier, Nopoulos et al. (2000, 2002, 2006) and Yang et al. (2012b) reported that populations with cleft may have differences in brain structure compared with craniofacially normal people. The present results support the suggestion that some patients with NSCL/P may have (C)APD related to such abnormalities, particularly given that the proportion of children with a history of middle ear disorder in both NSCL/P and control groups was small. FAPC was used in this study because it was developed for both parents/caregivers and teachers, and the results obtained could be compared with a previous study (Minardi et al., 2004). However, this questionnaire should be used with caution for (C)APD screening, and accurate subsequent diagnosis should be conducted through a comprehensive test battery that includes both objective and behavioral assessment tools. CONCLUSION The FAPC questionnaire responses from caregivers suggested that behaviors associated with (C)APD more commonly occurred in children with CP and children with CLP and were rarely found in craniofacially normal children and children with CL. Even when excluding the questionnaire item concerned with articulation problems, statistical differences between the results of children with CP and their craniofacially normal peers were shown, which implied children with NSCL/P may be at higher risk of (C)APD compared with craniofacially normal children. Behaviors related to auditory attention deficits and lack of learning motivation were the most typical problems reported by caregivers of children with NSCL/P in this study, along with poor academic performance. The results of this study provide evidence that, compared with craniofacially normal children, individuals with NSCL/P may not only be at risk of middle ear dysfunction related hearing disorder. A significant number of children have behavioral indications of (central) auditory processing disorder, particularly those children with CP and children with CLP. The auditory processing abilities of children with NSCL/P

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should be considered in order to potentially enhance their educational achievement and quality of life. Acknowledgments. The authors gratefully acknowledge the questionnaire translation work by the two Chinese translators. We would like to express our gratitude to the medical and nursing staff of the Cleft Lip and Palate Center, Beijing Stomatology Hospital, for their generous assistance during data collection. We appreciate the support of all the caregivers and children who participated in this study. The authors wish to thank the manuscript reviewers for their valuable suggestions and comments, which have improved the quality of this report. This research was supported by the Hong Kong Research Grants Council, General Research Fund (Grant No. 773009M).

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