Edited by: Mary Rudner, Linköping University, Sweden
Reviewed by: Dona M. P. Jayakody, Ear Science Institute Australia, Australia; Anita Eva Wagner, University Medical Center Groningen, Netherlands
This article was submitted to Language Sciences, a section of the journal Frontiers in Psychology
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Congenital cytomegalovirus (cCMV) infection is the most common cause of progressive hearing impairment. In our previous study around 90% of children with a cCMV infection and CI had severely damaged balance functions (Karltorp et al.,
This explorative follow-up study is part of a larger research program with the objective to investigate the effects of different etiological backgrounds in children with pediatric deafness. We have investigated the effects of congenital cytomegalovirus (cCMV) infection in a sample of deaf children with cochlear implants (CI), and results have been related to their executive functioning, pragmatic skills, mental health, and possible interactions with the participants' early language outcome. This has been done in a group of children with CI, deafened due to cCMV infection, and in hearing-matched controls with a genetic cause of deafness: Connexin 26 mutations (Cx26). Congenital CMV infection is known to be related to comorbid conditions, while Cx26 is usually not related to other issues or diagnoses.
Executive functions (EF) are connected to frontal lobe capacity (Kave et al.,
Some of the language variation in the population of children with CI may be explained by age at implantation (Dettman et al.,
The cause of deafness and comorbidity could contribute to explaining some of the still unknown variations in cognitive processing, including poorer EF, which can negatively influence pragmatic skills and/or mental health in preschool and school-aged children with CI. Goberis et al. (
Half of all sensorineural deafness (50%) is explained by genetic reasons (70% non-syndromic and 30% syndromic) (Alford et al.,
Congenital CMV infection has a birth rate of 5% per 1,000 births. It has previously been suggested that 80% of all infants who are infected with a CMV infection
There are several studies that have investigated spoken language in relation to EF abilities like phonological working memory in children with CI (Lyxell et al.,
We have previously reported that some children with cCMV can catch up and develop adequate speech and language abilities over time, while others may have comorbid conditions (Karltorp et al.,
Children with profound HI who use CI have been reported to have mental health issues more frequently than peers with TH (Hintermair,
Mental health can be assessed with the Strengths and Difficulties Questionnaire (SDQ), which was originally developed in nearly identical versions for parents and teachers of children aged 4–16 (Goodman,
The objective of the present study was to explore EF, pragmatic skills, and mental ill health in children with an acquired deafness (cCMV infection) using CI and who have no known additional diagnoses like ADHD, Developmental Language Disorder (DLD), or Autism-Spectrum-Disorder (ASD) and compare this to well-matched controls who were deafened due to a genetic non-syndromic deafness (Cx26 mutations). The groups were matched on the basis of age, hearing, vocabulary, parents' education level, and non-verbal cognitive ability.
Several research questions were addressed:
Do children with CI have Do children with a cCMV infection who use CI have Is there a relationship between EF, pragmatic skills, mental health, and early language abilities in children with CI, regardless of the cause of deafness?
The current follow-up study had a long-term approach, which included data collection and retrospective reviews of medical journals, and it is part of a larger research study program at the Auditory Implant Center, Karolinska Institutet, aiming to explore the effects of etiological factors in children with CI, who have different causes of deafness, in relation to their listening skills, cognitive abilities, mental health, and linguistic outcome. This study was carried out in accordance with the recommendations of the Regional Ethical Review Board in Stockholm, Sweden. All participants were first provided with written information about the study. Written informed consent was then obtained from the parents of all participants, in accordance with the Declaration of Helsinki. The protocol was approved by the Regional Ethical Review Board in Stockholm, Sweden; DN 2012:/2.
Inclusion criteria: children with cCMV or Cx26 who were older than 4 years and younger than 13 years at the time of the study, who used their CI during all waking hours, who did not have a confirmed and known additional diagnose(s) related to deficits in the domain of executive functioning (ASD, ADHD) or pragmatic skills (DLD, ASD), and who had at least one parent who spoke Swedish at home. Families with a child who fulfilled the criteria and who had been implanted at the Auditory Implant Center, Karolinska University Hospital, which covers half of the Swedish population (i.e., five million people), were invited to take part in the follow-up study. Parents were first provided with written information about the study and then, if interested, they were asked to sign an informed consent of participation form. Children who could read (older than 8 years) also signed a consent of participation. Seven children with cCMV were excluded because they were too young or too old, and two children with cCMV were excluded because they had several additional diagnoses aside from their deafness. There was one participant with Cx26 who fulfilled the criteria and who initially agreed to participate but later decided not to participate in the study.
The final study sample consisted of 17 children (
Participant demographics concerning ages (months) when individual children were identified with a hearing impairment (HI), ages at identification of cause of deafness (cCMV or Cx26), ages when the children received their 1st and 2nd CI; type of Family-Centered Early Intervention (FCEI) actions after identification of HI, and the chronological ages of the children at the follow-up study.
CMV-1 | 18 | 24 | 22 | 22 | 1 | 128 (10.7 year) |
CMV-2 | 13 | 24 | 17 | 72 | 1 | 82 (6.8 year) |
CMV-3 | 36 | 44 | 44 | 44 | 2 | 130 (11.0 year) |
CMV-4 | 0 | 10 | 12 | 12 | 1 | 106 (8.2 year) |
CMV-5 | 0 | 0 | 10 | 16 | 1 | 63 (5.3 year) |
CMV-6 | 6 | 16 | 17 | 39 | 2 | 67 (5.6 year) |
CMV-7 | 12 | 20 | 21 | 24 | 1 | 118 (9.8 year) |
CMV-8 | 0 | 18 | 18 | 30 | 2 | 155 (12.9 year) |
CMV-9 | 0 | 9 | 9 | 9 | 2 | 57 (4.8 year) |
CMV-10 | 30 | 64 | 67 | 3 | 81 (6.8 year) | |
Md (min-max) | 9 (0–36) | 19 (0–64) | 18 (9–67) | 24 (9–72) | 2 (1–3) | 99 (57–155) |
Cx26-11 | 2 | 10 | 8 | 49 | 1 | 108 (9.0 year) |
Cx26-12 | 2 | 52 | 48 | 2 | 70 (6.0 year) | |
Cx26-13 | 10 | 19 | 19 | 23 | 2 | 153 (12.8 year) |
Cx26-14 | 1 | 9 | 9 | 9 | 1 | 57 (4.8 year) |
Cx26-15 | 19 | 23 | 22 | 27 | 2 | 140 (11.8 year) |
Cx26-16 | 0 | 0 | 14 | 2 | 64 (5.3 year) | |
Cx26-17 | 2 | 22 | 34 | 95 | 2 | 93 (7.8 year) |
Md (min-max) | 2 (0–19) | 19 (0–52) | 19 (8–48) | 27 (9–95) | 2 (1–2) | 99 (57–155) |
All children (
All children (
All participating families had visited the same Auditory Implant Center at Karolinska University Hospital since their child received their first CI. Families were scheduled for a duration of around 4 h at the follow-up occasion (see
Description of assessment tools used at different test occasions in the study.
Reynell-III (Language understanding) | X | X | X | |
Expressive grammar scale | X | X | X | |
SIR-2 (Speech intelligibility) | X | X | X | |
BNT (expressive vocabulary) | X | |||
Lexical-semantic error analysis (BNT) | X | |||
FAS and Animal (word fluency ability) | X | |||
Ravens (non-verbal cognitive ability) | X | |||
TEA-Ch (attention level) | X | |||
EBA-R (observational analysis scale) | X | |||
SIPS; phonological working memory | X | |||
SIPS; general working memory | X | |||
Speech recognition (silence) | X | |||
Speech recognition (noise) | X | |||
BRIEF (parents) (EF skills) | X | |||
BRIEF (teachers) (EF skills) | X | |||
CCC-2 (parents) (pragmatics) | X | |||
SDQ (parent) (mental health) | X | |||
SDQ (teachers) (mental health) | X |
Everyday attention level was assessed with the Test of Everyday Attention for Children (TEA-Ch) in children older than 6 years (Heaton et al.,
Phonological working memory (a non-word repetition task that is a relatively pure measure of the phonological loop capacity, Baddeley,
Executive functioning in the home and a preschool/school environment was rated in a questionnaire by parents and the child's primary teacher, respectively, who filled in the Behavior Rating Inventory of Executive Function (BRIEF) to evaluate possible behavioral problems concerning EF in everyday settings (at home and in preschool/school, respectively) (Gioia et al.,
Emotional, Behavioral, and Attention Rating (EBA-R), an in-house developed observational and qualitative analysis scale (Henricson and Löfkvist,
The second edition of the Swedish version of the parent report questionnaire Child Communication Checklist (CCC-2) was used to examine the children's pragmatic skills (Bishop,
The SDQ is a 25-item screening questionnaire. Each item is rated 0 = not true, 1 = somewhat true, or 2 = certainly true (Goodman,
Sound field hearing thresholds were assessed by presenting frequency-modulated tones at octave frequencies from 0.125–6 kHz. The hearing tests were conducted using best-aided conditions (bilateral CI or in bimodal fashion; CI and HA) for speech in silence and in multi-source noise (Asp et al.,
All children were assessed with the Raven colored progressive matrices (Raven et al.,
Children were assessed by way of expressive vocabulary/picture naming by using a validated Swedish version of the Boston Naming Test (BNT) (Kaplan et al.,
The Reynell-III test evaluates expressive and receptive language abilities and was originally developed for children aged 0–7 years with TH (Edwards et al.,
Furthermore, experienced speech–language pathologists who were the same clinicians who performed the Reynell-III assessment pre-op, and after 1 and 3 years after the first CI, also rated the level of
The Speech Intelligibility Rating Scales (SIR-2) was specifically developed for use in children with HI and consists of a 5-level rating scale from “recognizable words in speech” to “connected speech is intelligible to all listeners” (Allen et al.,
Potential group differences (cCMV infection vs. Cx26) were examined with Mann Whitney U-tests that included effect size indicators;
We addressed three research questions in the current follow-up study that were related to possible similarities and differences in EF outcome, pragmatics, and mental health in a sample of deaf children with CI and with different etiological backgrounds. The groups (cCMV and Cx26) were initially matched based on age, hearing (CI), vocabulary (BNT; raw scores), and non-verbal cognitive ability (Ravens matrices). There were no statistically significant differences between groups (cCMV and Cx26) regarding the speech recognition outcome (
Early speech, language, and hearing outcome (pre-op, post-op after 1 and 3 years with 1st CI), and age at walking (months), on group level (cCMV infection and Cx26 mutations), including statistical values for group comparisons (Mann Whitney
Pre-op | 0 (0–1), ( |
0 (0–42) | −1.01 | 0.25 | |
1-year post-op | 13 (3–43), ( |
25 (17–53), ( |
−1.89 | 0.49 | |
3- years post-op | 47 (37–52), ( |
51 (51–54), ( |
−2.09 | 0.56 | |
Pre-op | 1 (1–5) | 1 (1–4) | −0.69 | 0.17 | |
1-year post-op | 2 (2–3), ( |
3 (2–4), ( |
−1.86 | 0.45 | |
3-years post-op | 4 (2–5), ( |
5 (4–5) | −2.08 | 0.50 | |
Pre-op | 2 (1–8) | 2 (1–7) | −0.41 | 0.10 | |
1-year post-op | 6 (4–7), ( |
6 (5–8), ( |
−1.05 | 0.27 | |
3-year post-op | 7 (7–8), ( |
8 (7–8) | −1.39 | 0.34 | |
18 (12–23), ( |
12 (11–13) | −3.05 | 0.76 |
There was one statistically significant difference between children with cCMV and children with Cx26 on the phonological working memory test (
Attention level was assessed with the TEA-Ch test in all children older than 6 years. Although, there were only six children with cCMV and four children with Cx26, one statistically significant difference was found on one subscale; “walk don't walk” targets impulse control under time pressure (
There were no statistically significant group differences on any of the scales: Expression of positive emotions; Frustration level (
The group median results of the BRIEF rating indicated slightly worse results than expected in relation to norm data for children with TH, but there was a large variation within the cCMV group. The majority of children with cCMV were within limits of typical levels compared to American norm data. We found no statistically significant group differences (cCMV and Cx26) (
Although there was some variation in outcome between individuals within the Cx26-group, there was no child with genetic deafness who reached a t-score over 65 on either the BRI, MI, or GEC, indicating that children with Cx26 were within typical levels for children with TH in the same ages (norms). This suggests that children with Cx26 deafness did not have specific EF problems at home or in preschool/school. One child with Cx26 had results that scored higher than average on working memory and shifting (two subscales in BRIEF), which means that this child could have slightly worse results than expected, but not clinically atypical (see
To summarize, our first hypothesis that children with CI in both groups (cCMV and Cx26) had worse EF outcomes than children with TH was only partly confirmed by these pilot results. Children with cCMV had statistically significant worse phonological memory abilities than children with Cx26. Due to the small sample size and missing data from the TEA-Ch test we could not conclude that children with cCMV had substantially poorer attention and impulse control than children with Cx26 mutations. Three individuals with cCMV had BRIEF results that indicated they should be referred to a clinical psychologist for a more thorough investigation of their EF, while there were none in the control group with similar indications.
Results on the parent questionnaire CCC-2, measuring the child's pragmatic skills, showed significant differences between groups (cCMV infection and Cx26) on the IGK/total raw score (
All children in the sample, with a few exceptions, had typical results on mental health (SDQ) compared to norm data (
Language, non-verbal cognition and hearing outcome measures (median, range, and statistical values), compared on group level (cCMV vs. Cx26), including the effect sizes.
Raw scores | 31 (0–46)∞ | 34 (23–53) | −0.82 | 0.05 | |
Stanine | 4 (1–9)∞ | 3 (1–9) | −0.48 | 0.02 | |
Semantic relevant errors | 11 (6–24)∞ | 11 (6–22) | −0.42 | 0.01 | |
Semantic irrelevant errors | 11 (3–22)∞ | 10 (0–21) | −0.53 | 0.07 | |
No responds | 0 (0–13)∞ | 0 (0–8) | −0.14 | <0.01 | |
Total numbers | 18 (0–34) | 13 (1–37) |
−0.20 | <0.01 | |
Total numbers | 13 (2–19) | 10 (7–17) | −0.33 | <0.01 | |
Raw scores | 25 (14–34) | 32 (14–35) | −1.36 | 0.12 | |
Quiet (%) | 84 (64–100)§ | 68 (48–100) | −0.83 | 0.05 | |
Noise (%) | 50 (32–68) × | 56 (32–68)¤ | −0.52 | 0.02 |
Mental health.
F | 6 (2–12) | 3 (0–7) | −1.75 | 0.44 | ||
M | 6 (0–12) | 3 (0–9) | −1.01 | 0.25 | ||
T | 4 (0–16) | 3 (0–10) | 0.00 | – | ||
F | 0 (0–2) | 1 (0–2) | −1.01 | 0.25 | ||
M | 0 (0–3) | 1 (0–4) | −1.74 | 0.44 | ||
T | 4 (0–16) | 0 (0–3) | −0.86 | 0.22 | ||
F | 2 (0–3) | 0 (0–1) | −2.23 | 0.56 | ||
M | 1 (0–3) | 0 (0–3) | −0.82 | 0.21 | ||
T | 0 (0–3) | 0 (0–2) | −0.15 | 0.04 | ||
F | 3 (1–6) | 0 (0–1) | −1.51 | 0.38 | ||
M | 3 (0–8) | 0 (0–5) | −1.39 | 0.35 | ||
T | 2 (0–10) | 2 (0–7) | −0.89 | 0.22 | ||
F | 1 (0–3) | 0 (0–1) | −2.12 | 0.53 | ||
M | 0 (0–5) | 0 (0–1) | −0.42 | 0.11 | ||
T | 0 (0–2) | 0 (0–1) | −0.43 | 0.11 | ||
F | 8 (6–10) | 10 (7–10) | −1.94 | 0.49 | ||
M | 9 (7–10) | 10 (8–10) | −0.88 | 0.22 | ||
T | 7 (5–10) | 9 (2–10) | −0.07 | 0.02 |
The second hypothesis we had before the study was that children with cCMV would have worse pragmatic skills than hearing-matched controls due to (presumed) worse executive functioning. The results showed statistically significant differences between groups (cCMV and Cx26), both on total raw score and on subscales that are related to conversational skills (initiatives and use of context); both are important for social cognition and could be related to
There were some correlations among EF, pragmatic skills, mental health, and level of language understanding and speech intelligibility rating after 3 years with the first CI, and these are presented in
Correlation coefficients for EF skills, pragmatics and mental health rated by mothers and fathers, and early language abilities after 3 years with 1st CI; language understanding (Reynell-III) and speech intelligibility (SIR-2), for children with cCMV and Cx26.
1. Phonological WM | – | −0.56 |
0.61 |
0.55 | 0.39 | −0.48 | −0.65 |
2. EF skills, GEC (BRIEF) | – | −0.58 |
−0.42 | −0.34 | −0.70 |
0.38 | |
3. Pragmatics (CCC-2) | – | 0.74 |
0.63 |
−0.73 |
−0.63 |
||
4. Language understanding |
– | 0.65 |
−0.48 | −0.48 | |||
5. Speech intelligibility (SIR-2) | – | -32 | −0.43 | ||||
6. SDQ, total score, M | – | 0.65 |
|||||
7. SDQ, total score, F | – |
One initial hypothesis was that there would be a relationship between EF, pragmatic skills, and mental health in all children with CI, regardless of their cause of deafness, and that better speech and language understanding in early childhood would be related to better outcomes in pragmatics, EF, and social behavior in later childhood (Goberis et al.,
In this follow-up study of children with cCMV compared to well-matched controls, we started with three research questions that arose after previous findings indicated that children with cCMV might have specific EF difficulties, which could affect their social or pragmatic development/behavior (Karltorp et al.,
On a group level, children with cCMV did have statistically significant worse phonological working memory than matched controls, but there was no group difference on general working memory. This indicates group-specific differences in how linguistic information is processed. Children with cCMV appeared to find it especially more difficult to process phonologically based information without semantic clues than children with Cx26. The children in the whole sample showed variation in the vocabulary outcome, but there were no statistically significant subgroup differences regarding the vocabulary size (total score on BNT) or the lexical-semantic error response analysis. Children with cCMV performed well on the FAS letter-fluency task, which means that children in the sample (on a group level) had sufficient and effective strategies to learn words and retrieve lexical-semantic information from their long-term memory despite the fact that they also had a worse ability to process non-words (Löfkvist et al.,
Some individuals with a cCMV infection did not complete all the tests, due either to fatigue or for unknown reasons, while children with Cx26 did not complain about fatigue in the same way, indicating worse
Children with CI, regardless of their cause of deafness, had more or less typical mental health results that were comparable to norm data of age-matched children with TH, which is a positive result. Only two aspects related to mental health differed in the two subgroups. Fathers reported conduct problems and poor peer functioning in children with cCMV compared to the hearing-matched controls with Cx26, which could be related to worse EF (Lyxell et al.,
There were statistically significant differences between groups on the total score of the pragmatic skills questionnaire (CCC-2) as well as for the subscales
Most et al. (
The fathers in the current study reported statistically significant less-well conduct levels and peer problems in the cCMV infection group compared to controls. These two functions are interrelated and associated with social behavior. Poor behavior could lead to affected peer relations. Conduct level might also be related to pragmatics (Goberis et al.,
The participating children in the two groups were initially matched based on age, hearing-level, vocabulary knowledge, non-verbal cognitive ability, home language situation (at least one parent who speak Swedish), and no other known additional diagnoses besides the deafness. Furthermore, at the time of the follow-up study we found no differences between groups based on socio-economic status (parental education level). Nonetheless, there were some significant statistical group differences between children that were related to their early childhood. Children with cCMV on average started to walk later than children with Cx26, which is suggestive of a balance problem that has been reported on before (Karltorp et al.,
Another difference between groups (cCMV and Cx26) in the current study was their early daycare environment. All but one child with Cx26 went to mainstream daycare from the start and continued to be mainstreamed onwards, while some children with cCMV infection had initially attended special units for deaf and hearing-impaired children, with more exposure to sign language and total communication, before they changed to mainstream preschools/schools. All participants with cCMV had parents who were TH; all children with cCMV therefore had access to spoken language throughout their early childhood in their home environment. We therefore have no reason to believe that the initial different daycare settings would explain later group differences in EF abilities or language outcome, including their pragmatic skills. The worse spoken language understanding level after 3 years with CI in children with cCMV infection could potentially be related to limited exposure of spoken language in daycare, but is more likely explained by previous findings that there is a slower pace in speech and language development in children with cCMV compared to other subgroups of children with CI (Ramirez Inscoe and Nikolopoulos,
Although the present study was limited in the number of individuals, the pilot study contributed with new knowledge about executive functioning, pragmatic skills, and mental health in deaf children with cCMV who use CI as well as for matched controls with Cx26 mutations. Future studies should look more closely into individual results in children with a cCMV infection. It would be beneficial to conduct a study with a longitudinal study design to further examine the developmental aspects of executive functions and pragmatic skills and include theory-of mind as an aspect in relation to the children's mental health, including their own self-perceived opinion and perspectives. Comparative cross-sectional studies should include more participants with cCMV and controls with TH who are matched based on age and socio-economic status and preferably also including a control group of typically hearing children with ADHD.
To conclude, children with a cCMV infection who used CI, and who did not have previous known diagnoses like ADHD, DLD, or ASD, had worse pragmatic skills and phonological working memory compared to well-matched controls with Cx26 and CI. Both groups with CI had typical mental health according to parent and teacher reports; some fathers' reports, however, showed more conduct problems and poor peer functioning in the group of children with cCMV infection. Parents and teachers did not report severe EF difficulties in everyday settings on group level. Better early language skills after 3 years of CI use was correlated to better pragmatic skills and mental health at later ages. The results indicate that it is important to identify children with cCMV as early as possible and support them and their families with preventive language stimulation actions, including specific training of social and pragmatic skills. Besides listening and language abilities, social cognition and EF should be assessed on a regular basis. This might limit the risk that subgroups like children with cCMV are left behind in social interaction and learning situations.
The datasets generated for this study are available on request to the corresponding author.
This study was carried out in accordance with the recommendations of the Regional Ethical Review Board in Stockholm, Sweden. All participants were first provided with written information about the study. Then a written informed consent was obtained from the parents of all participants, in accordance with the Declaration of Helsinki. The protocol was approved by the Regional Ethical Review Board in Stockholm, Sweden; DN 2012:/2.
All authors contributed with planning of the study, conducted the data collection, and performed data analysis/interpretation as well as discussed results and commented on the manuscript at all stages. UL conducted most of the statistical analysis as well as prepared the draft.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The handling editor declared a shared affiliation, though no other collaboration, with one of the authors CH at the time of the review.
The Supplementary Material for this article can be found online at: