The Laryngoscope C 2014 The American Laryngological, V
Rhinological and Otological Society, Inc.
Evidence for a Right Cochlear Implant Advantage in Simultaneous Bilateral Cochlear Implantation Yael Henkin, PhD; Riki Taitelbaum Swead, PhD; Daphne Ari-Even Roth, PhD; Liat Kishon-Rabin, PhD; Yisgav Shapira, MD; Lela Migirov, MD; Minka Hildesheimer, PhD; Ricky Kaplan-Neeman, PhD Objectives/Hypothesis: To compare speech perception performance with right versus left cochlear implants (CIs) in children with bilateral CIs implanted simultaneously. Study Design: Prospective case series of patients undergoing simultaneous bilateral cochlear implantation. Methods: Speech perception performance was tested in 10, right-handed children who received bilateral CIs simultaneously between 11 and 36 months (mean, 21 months), had at least 18 months of bilateral CI use, and were 5.3 years of age during testing. All children exhibited bilateral symmetrical severe-to-profound hearing loss prior to implantation and did not benefit from hearing aids. Speech perception performance was evaluated with the right CI and the left CI by means of an open-set monosyllabic word test in quiet presented at 45 dB HL in a sound field. Results: All children exhibited higher performance with the right CI compared to the left CI. Group mean performance with the right CI was 66.5% compared to 52% with the left CI (P 5.002), yielding a 14.5% difference. With increasing duration of bilateral CI use and age at evaluation, the right–left difference increased (r 5 0.72, P 5.019 and r 5 0.74, P 5.014, respectively). Conclusions: Current preliminary data indicate that children with bilateral CIs implanted simultaneously exhibit a significant right ear advantage for speech. Similarly to reports on normal-hearing children, right ear preference for speech increased with increasing age and auditory–linguistic experience. Thus, simultaneous bilateral cochlear implantation may lead to normal development of auditory pathways and may be an important contributor to the superior auditory, language, and communication skills reported in children with bilateral versus unilateral CIs. Key Words: Cochlear implant, bilateral simultaneous cochlear implantation, right ear advantage, speech perception, children. Level of Evidence: 4. Laryngoscope, 124:1937–1941, 2014
INTRODUCTION Over two decades of experience have shown that unilateral cochlear implants (CIs) substantially improve sound and speech perception thereby promoting development of speech, language, and communication skills.1–3 Despite these benefits, unilaterally implanted children are denied of the binaural advantages including summation, redundancy, squelch, and have limited access to interaural time and level differences. In addition, maximal benefit from the head shadow effect is restricted. From the Department of Communication Disorders (Y.H., D.A.-E.R., Sackler Faculy of Medicine, Tel Aviv University, Tel Aviv; and the Hearing, Speech, and Language Center (Y.H., R.T.S., D.A.-E.R., M.H., R.K.-N.), and Department of Otolaryngology–Head and Neck Surgery (Y.S., L.M.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel. Editor’s Note: This Manuscript was accepted for publication January 24, 2014. This work was performed at the Department of Communication Disorders, Sackler Faculy of Medicine, Tel Aviv University, and the Hearing, Speech, and Language Center, Sheba Medical Center, Tel Hashomer, Israel. The authors have no funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Yael Henkin, PhD, Department of Communication Disorders, Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel 52621. E-mail: [email protected] L.K.-R., M.H., R.K.-N.),
DOI: 10.1002/lary.24635
Laryngoscope 124: August 2014
Consequently, they exhibit difficulties in speech understanding in noise4 and sound localization5,6 and may show inferior expressive and receptive language skills7,8 compared to those of bilaterally implanted children and normal-hearing peers. In an attempt to diminish the negative effects of unilateral auditory deprivation and provide deaf children with binaural advantages, there is an increasing trend toward bilateral cochlear implantation. A recent worldwide survey indicated that 70% of bilateral implantations occur in children, with the highest representation of the 3- to 10-year-old age group (33% of all bilateral implantations), and children under 3 years (26%).9 In most cases, bilateral implants are provided sequentially, with variable periods between the first and second implantation. Nonetheless, there is growing agreement that “the infant or child with unambiguous cochlear implant candidacy should receive bilateral cochlear implants simultaneously as soon as possible after definitive diagnosis of deafness to permit optimal auditory development” (European Bilateral Pediatric Cochlear Implant Forum consensus statement).10 Although current guidelines have substantially reduced the minimal age at implantation, congenitally deaf children continue to experience various periods of bilateral and unilateral auditory deprivation prior to Henkin et al.: Right Ear Advantage and Bilateral CIs
1937
implantation, which may affect normal neurodevelopment and lead to reorganization of the central auditory system.11,12 In the normal auditory system, numerous functional imaging, electrophysiological, and behavioral studies have shown that although the auditory cortex receives sensory input from both ears, it is excited most strongly by stimulation of the contralateral ear.13–17 When stimulated by speech, stronger contralateral activation is manifested in the “right ear advantage” phenomenon using dichotic listening tasks, and is ascribed to stronger crossed auditory pathways from the right ear ascending to the speech-dominant left hemisphere.18 This asymmetry has been exhibited through the lifespan, from 4-day-old neonates19,20 to adulthood,21–25 to various speech stimuli (e.g., consonant–vowel syllables, stop consonants, and words).26–28 Recently published data indicate that unilateral cochlear implantation may alter the development of normal auditory pathways and result in cortical reorganization11,29; nevertheless, limited data exist regarding ear advantage patterns in unilateral CI recipients. Based on the well-substantiated right ear advantage for speech in normal-hearing listeners, it was speculated that the right ear should be the preferred ear for implantation30 in an attempt to maximize speech perception performance. This assertion has been tested in postlingually deafened adults and in prelingually deafened children, all implanted unilaterally. Data suggest that postlingually deafened elderly CI recipients implanted in the right ear outperformed those implanted in the left ear in speech perception tests in quiet (words) and in noise (sentences).31 Nonetheless, the right CI advantage was not evident in young postlingually deafened adults, with right versus left CI showing similar improvement on speech perception tests by 12 months of implant use.32 In prelingually deafened children, we reported data from a cohort of 71 children, 30 implanted in the right and 41 implanted in the left, indicating a slight yet significant right CI advantage that was evident throughout a 3-year follow-up and was independent of age at implantation.33 These results are in keeping with our earlier electrophysiological data showing differential brain activation patterns during speech processing in children with right versus left CI.34 Based on the recording of the P3 event-related potential known to reflect discrimination and categorization of stimuli, children implanted in the right ear exhibited bilateral temporal and frontal lobe activation while processing consonant–vowel syllables, similarly to normal-hearing controls. In contrast, children implanted in the left ear showed differential patterns characterized by enhanced ipsilateral temporal lobe activation. Following this line of investigation, we asked whether a right CI advantage for speech is evident in children with bilateral CI implanted simultaneously. The working premise was that children who experienced relatively short duration bilateral auditory deprivation and received simultaneous bilateral cochlear implants thereafter, may exhibit a right CI advantage for speech. For this purpose, we studied a group of children with bilateral CI who were implanted simultaneously, had substantial duration of CI use, and could fully cooperate in a speech perception test. Laryngoscope 124: August 2014
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MATERIALS AND METHODS Subjects Among the 497 children who were implanted at Sheba Medical Center, Tel Hashomer, between 1991 and 2013, 147 (30%) were implanted bilaterally. Of these, 48 received bilateral CIs simultaneously between 2007 and 2013, with the majority implanted between 2010 and 2013. Among the simultaneously implanted children, 10 children who were old enough to cooperate in speech perception testing and had at least 18 months of bilateral CI use participated in the study. They were implanted between 11 and 36 months of age (mean, 21.2 months) and used their CIs regularly for 18 to 75 months (mean, 44.2 months). Individual background information is presented in Table I. All children were diagnosed with bilateral severe-to-profound sensory neural hearing loss based on auditory brainstem response measurements and behavioral testing, and were habilitated bilaterally with high-power digital hearing aids shortly after diagnosis. They showed limited benefit from hearing aids as detailed in Table I. All were healthy, right-handed based on parental report, with fully inserted electrodes, and without cochlear malformations based on radiographic evaluation. All children were using oral communication and mainstreamed in regular educational settings. Seven children were congenitally deaf, whereas three children were deafened as a result of meningitis at 27, 33, and 20 months (Table I, subjects 1, 3, and 7, respectively). These three children were implanted 3, 4, and 6 months postmeningitis, respectively. Postoperative reports indicated complete cochlear ossification in the right ear and partial ossification in the left ear in patient 3, partial ossification in the basal turn especially in the right ear in patient 1, and no ossification in patient 7. The age at testing of all children ranged between 30 and 108 months (mean, 64.3 months). Seven children were implanted with MedEl devices, two with Cochlear devices, and one with Advanced Bionics devices. All electrodes were activated in all patients excluding three patients using MedEl devices: patient 3, electrode 12 bilaterally; patient 1, electrode 12 (left); patient 10, electrode 12 (right) and 11 (left).
Test Measures Speech perception was evaluated using the prerecorded Hebrew version of the Arthur Boothroyd (AB)35 open-set monosyllabic, consonant–vowel–consonant word recognition test. Based on clinical experience, the Hebrew AB test can be administered to young children. Two lists of AB words were presented in each of the two listening conditions, right CI and left CI, in random order. The words were presented at 45 dB HL in free field via two loudspeakers located at 45 on the right and left, at a distance of 1 m from the subject.
Statistical Methods The nonparametric Wilcoxon signed rank test was used to evaluate the difference in performance in the Hebrew AB test between the right and left CIs, as it was unlikely to be normally distributed. Furthermore, correlation between the right–left CI difference in performance and 1) age at implantation, 2) age at evaluation, and 3) duration of CI use, was evaluated by means of Pearson correlation coefficients.
RESULTS Aided thresholds, as measured by voice detection levels and speech reception thresholds with the right and left CIs, were comparable (P 5.25 and P 5.2, respectively) and are depicted in Figure 1. Henkin et al.: Right Ear Advantage and Bilateral CIs
TABLE I. Background Information of CI Recipients. Preimplantation ABR Thresholds to Clicks, 0.5, and 1 kHz Tone Bursts, dB nHL Patient
Etiology of Deafness
Aided VDL, dB HL*
Right
Left
Right
Left
Age at Implantation, mo
CI Devices
Duration of CI Use, mo
Age at Evaluation, mo
1
Meningitis
NR, NR, NR
NR, NR, NR
90
90
30
MedEl
75
105
2 3
Genetic Meningitis
NR, 90, NR NR, 80, NR
NR, NR,NR NR, 80, NR
45 55
40 55
12 36
MedEl MedEl
18 72
30 108
4
Unknown
NR, NR, NR
85, NR, NR
70
70
35
Cochlear
18
53
5 6
Genetic Genetic
NR, NR, NR NR, NR, NR
NR, NR, NR NR, NR, NR
60 100
70 100
15 12
MedEl Cochlear
48 18
63 30
7
Meningitis
NR, NR, NR
NR, NR, NR
75
55
26
MedEl
57
83
8 9
Connexin 26 Waardenburg
NR, NR, 100 NR, NR, NR
NR, NR, NR NR, NR, NR
30 80
55 60
11 13
MedEl Advanced Bionics
52 48
53 60
10
Genetic
NR, NR, NR
NR, NR, NR
90
90
22
MedEl
36
58
*Aided voice detection levels (VDL) in free field with hearing aids. ABR 5 auditory brainstem response; CI 5 cochlear implant; NR 5 no response at maximum output.
Figure 2 shows individual performance in the AB test with the right and left CIs and group mean data. For all participants, performance with the right CI was higher than with the left CI. Group mean performance was significantly higher with the right CI (66.5%) compared with the left CI (52%) (P 5.002) yielding a 14.5% difference. Three children who were deafened as a result of meningitis showed a larger right–left difference of 20%, 30%, and 20% (subjects 1, 3, and 7, respectively) compared to the seven prelingually deafened children who showed a mean difference of 10.7% (range, 5%–20%). Testing the right–left difference in the seven prelingually deafened children, yielded a significant right CI advantage (P 5.016).
Fig. 1. Group mean aided voice detection levels (VDL) and speech reception thresholds (SRT) with the right (Rt) and left (Lt) cochlear implants.
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The right–left difference in performance was strongly correlated with 1) age at evaluation (r 5 0.74, P 5.014) and 2) duration of implant use (r 5 0.72, P 5.019). These correlations are depicted in Figures 3 and 4 showing that with increasing age at evaluation and duration of CI use, the right–left difference increased. The correlation between the right–left difference and age at implantation was moderate yet did not reach significance (r 5 0.54, P 5.1).
DISCUSSION The current study provides first-time preliminary evidence indicating a significant right CI advantage of
Fig. 2. Individual and group mean speech perception performance with the right (Rt) and left (Lt) cochlear implants (CI).
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Fig. 3. Right (Rt)–left (Lt) difference in performance as a function of age at evaluation. Note that with increasing age at evaluation, the right–left difference increases. CI 5 cochlear implant.
14.5% for speech in right-handed children with bilateral CIs implanted simultaneously at a young age. It is plausible that for this small group of children, all exhibiting a right CI advantage, simultaneous stimulation of auditory pathways resulted in the restoration of normal asymmetry. Support for this notion is provided by recent data collected by Gordon et al.11 showing that cortical activity, manifested by the P1 potential to biphasic electrical pulses in children who were implanted simultaneously or sequentially with short interimplant delay (2 years) showed a different pattern characterized by enhanced ipsilateral activation. Based on this finding, the authors concluded that bilateral auditory stimulation provided with limited delay can protect the brain from irreversible reorganization found in unilaterally implanted children or sequentially implanted children with long interimplant delay. Data regarding cortical activation patterns to speech stimuli are required to further clarify lateralization patterns to speech in CI recipients. The perceptual asymmetry found in the present study in CI recipients is not evident in normal-hearing listeners while performing monaural speech recognition tasks in quiet due to a ceiling effect. Typically, the right ear advantage is exhibited in normal-hearing listeners by means of dichotic listening tasks.25 Increased task difficulty and stimuli uncertainty, however, were also found to demonstrate this phenomenon.36 For example, competing monaural stimulation of words resulted in a substantial right ear advantage.37 For CI recipients, monaural speech recognition tasks with low linguistic redundancy (i.e., monosyllabic words), even in quiet, are challenging and may therefore suffice to demonstrate the CI side advantage. Support for this notion is the remarkably similar magnitude of the right CI advantage found in children with bilateral CI implanted simultaneously in the current study (14.5%) and that found in Laryngoscope 124: August 2014
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unilaterally implanted recipients with right versus left CI while performing a monosyllabic word test in quiet (children: 13.7%33, elderly adults: approximately 13%31). It should further be noted that the right CI advantage was persistent over 2 and 3 years of follow-up in children and in elderly adults, as reported by Henkin et al.33 and Budenz et al.,31 respectively. Increased contralateral lateralization of cortical activity (during the P1 potential) toward the linguistically dominant left hemisphere in children with unilateral right CI,11 together with data showing similar bilateral activation (during the P3 potential) to speech sounds in children with right CI and normal-hearing peers,34 may elucidate the differences in performance between children with a right and left CI.33 Interestingly, the right CI advantage was more prominent in three perilingually deafened children who suffered meningitis at 20, 27, and 33 months and were implanted shortly thereafter (3–6 months), compared to the remaining seven children who were all prelingually deafened and implanted at a mean age of 17 months. The meaning of the magnitude of the right CI advantage in a monaural speech perception task in quiet is unclear. Nonetheless, the more pronounced right–left difference in the perilingual children (23%) compared to the prelingual children (11%) may reflect substantial time in sound and exposure to language prior to loss of hearing, together with their older age at evaluation. For the currently studied group, the duration of CI use and age at evaluation were strongly correlated with the right–left difference. In other words, with increasing duration of implant use from 18 to 75 months and increasing age at evaluation from 30 to 108 months, the right CI preference increased. This finding is in agreement with dichotic listening data from normal-hearing right-handed children showing that the right ear preference for verbal material increased with age from 7 to 13 years.37,38 It has been suggested that developmental increases in attention, working memory, and language skills may enlarge the magnitude of ear advantage.25,39
Fig. 4. Right (Rt)–left (Lt) difference in performance as a function of duration of bilateral cochlear implant (CI) use. Note that with increasing duration of bilateral CI use, the right–left difference increases.
Henkin et al.: Right Ear Advantage and Bilateral CIs
Finally, recent data from a multicenter study show superior expressive and receptive language skills in 25 children with bilateral CI compared to carefully matched children with unilateral CI after 3 years of CI use. Moreover, eight children who were implanted simultaneously achieved higher expressive word development scores compared to those who were implanted sequentially. It is reasonable to assume that improved sound localization and speech perception in quiet and in challenging listening environments reported for children with bilateral CI facilitates incidental learning that is crucial for normal language development. Moreover, it is plausible that simultaneous bilateral cochlear implantation led to normal development of auditory pathways and restored the right ear advantage for speech that is typical in the presence of normal hearing.
CONCLUSION Current preliminary data indicate that children with bilateral CIs implanted simultaneously exhibited a significant right ear advantage for speech presented monaurally in quiet. Similarly to reports on normal-hearing children, right ear preference for speech increased with increasing age and auditory–linguistic experience. Thus, simultaneous bilateral cochlear implantation may lead to normal development of auditory pathways and may be an important contributor to the superior auditory, language, and communication skills reported in children with bilateral versus unilateral CI.
BIBLIOGRAPHY 1. Svirsky MA, Teoh SW, Neuburger H. Development of language and speech perception in congenitally, profoundly deaf children as a function of age at cochlear implantation. Audiol Neurootol 2004;9:224–233. 2. McConkey Robbins A, Koch DB, Osberger MJ, Zimmerman-Phillips S, Kishon-Rabin L. Effect of age at cochlear implantation on auditory skill development in infants and toddlers. Arch Otolaryngol Head Neck Surg 2004;130:570–574. 3. Peterson NR, Pisonia DB, Miyamoto RT. Cochlear implants and spoken language processing abilities: Review and assessment of the literature. Restor Neurol Neurosci 2010;28:237–250. 4. Culling FJ, Jelfs S, Talbert A, Grange JA, Backhouse SS. The benefit of bilateral versus unilateral cochlear implantation to speech intelligibility in noise. Ear Hear 2012;33:673–682. 5. Litovsky RY. Review of recent work on spatial hearing skills in children with bilateral cochlear implants. Cochlear Implants Int 2011;12(suppl 1):S30–S34. 6. Grieco-Calub TM, Litovsky RY. Spatial acuity in 2-to-3-year-old children with normal acoustic hearing, unilateral cochlear implants, and bilateral cochlear implants. Ear Hear 2012;33:561–572. 7. Boons T, Brokx JP, Frijns JH, et al. Effect of pediatric bilateral cochlear implantation on language development. Arch Pediatr Adolesc Med 2012; 166:28–34. 8. Davidson LS, Geers AE, Nicholas JG. The effects of audibility and novel word learning ability on vocabulary level in children with cochlear implants [published online ahead of print August 30, 2013]. Cochlear Implants Int doi: 10.1179/1754762813Y.0000000051. 9. Peters BR, Wyss J, Manrique M. Worldwide trends in bilateral cochlear implantation. Laryngoscope 2010;120:S17–S44. 10. Ramsden JD, Gordon K, Aschendorff A, et al. European Bilateral Pediatric Cochlear Implant Forum consensus statement. Otol Neurotol 2012;33: 561–565.
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11. Gordon KA, Wong DE, Papsin BC. Bilateral input protects the cortex from unilaterally-driven reorganization in children who are deaf. Brain 2013; 136:1609–1625. 12. Gilley PM, Sharma A, Dorman MF. Cortical reorganization in children with cochlear implants. Brain Research 2008;1239:56–65. 13. Langers DRM, van Dijk P, Backes WH. Lateralization, connectivity and plasticity in the human central auditory system. Neuroimage 2005;28: 490–499. 14. Scheffler K, Bilecen D, Schmid N, et al. Auditory cortical responses in hearing subjects and unilateral deaf patients as detected by functional magnetic resonance imaging. Cereb Cortex 1998;8:156–163. 15. Suzuki M, Kitano H, Kitanishi T, et al. Cortical and subcortical activation with monaural monosyllabic stimulation by functional MRI. Hear Res 2002;163:37–45. 16. Ponton CW, Vasama JP, Tremblay K, et al. Plasticity in the adult human central auditory system: evidence from late-onset profound unilateral deafness. Hear Res 2001;154:32–44. 17. Khosla D, Ponton CW, Eggermont JJ, et al. Differential ear effects of profound unilateral deafness on the adult human central auditory system. J Assoc Res Otolaryngol 2003;4:235–249. 18. Kimura D. Cerebral dominance and the perception of verbal stimuli. Can J Psychol 1961:15:166–171. 19. Bertoncini J, Marais J, Bueliac-Babic R, et al. Dichotic perception and laterality in neonates. Brain Lang 1989;37:591–605. 20. Dehaene-Lambertz G, Hertz-Pannier L, Dubois J. Nature and nurture in language acquisition: anatomical and functional brain imaging-studies in infants. Trends Neurosci 2006;29:367–373. 21. Bryden MP, Munhall K, Allard F. Attentional biases and right-ear effect in dichotic listening. Brain Lang 1983;18:236–248. 22. Hiscock M, Inch R, Kinsbourne M. Allocation of attention in dichotic listening: differential effects on the detection and localization of signals. Neuropsychology 1999;13:404–414. 23. Branccuci A, San Martini P. Laterality in the perception of temporal cues of musical timbre. Neuropsychologia 1999;37:1445–1451. 24. Moncrieff DW, Wilson RH. Recognition of randomly presented one-, two-, and three-pair dichotic digits by children and young adults. J Am Acad Audiol 2009;20:58–70. 25. Moncrieff DW. Dichotic listening in children: age-related changes in direction and magnitude of ear advantage. Brain Cogn 2011;76: 316–322. 26. Schwartz J, Tallal P. Rate of acoustic change may underlie hemispheric specialization for speech perception. Science 1980;207:1380–1381. 27. Spellacy F, Blumstein S. The influence of language set on ear preference in phoneme recognition. Cortex 1970;6:430–439. 28. Studdert-Kennedy M, Shankweiler D. Hemispheric specialization for speech perception. J Acoust Soc Am 1970;48:579–594. 29. Kral A, Hubka P, Heid S, Tillein J. Single-sided deafness leads to unilateral aural preference within an early sensitive period. Brain 2013;136: 180–193. 30. Roman S, Canevet G, Lorenzi C, et al. Voice onset time encoding in patients with left and right cochlear implants. Neuroreport 2004;14:601– 605. 31. Budenz CL, Cosetti MK, Coelho DH, et al. The effects of cochlear implantation on speech perception in older adults. J Am Geriatr Soc 2011;59: 446–453. 32. Morris LG, Mallur PS, Roland JT Jr, Waltzman SB, Lalwani AK. Implication of central asymmetry in speech processing on selecting the ear for cochlear implantation. Laryngoscope 2007;117:939–943. 33. Henkin Y, Taitelbaum-Swead R, Hildesheimer M, Migirov L, Kronenberg J, Kishon-Rabin L. Is there a right cochlear implant advantage? Otol Neurotol 2008;29:489–494. 34. Henkin Y, Kishon-Rabin L, Tatin-Schneider S, Urbach D, Hildesheimer M, Kileny PR. Low-resolution electromagnetic tomography (LORETA) in children with cochlear implants: a preliminary report. Int J Audiol 2004;43(suppl 1):S48–S51. 35. Boothroyd A. Statistical theory of speech discrimination score. J Acoust Soc Am 1968;43:362–367. 36. Geffen G, Quinn K. Hemispheric specialization and ear advantages in processing speech. Psychol Bull 1984;96:273–291. 37. Bradshaw JL, Farrelly J, Taylor MJ. Synonym and antonym pairs in the detection of dichotically and monaurally presented targets: competing monaural stimulation can generate a substantial right ear advantage. Acta Psychol 1981;47:189–205. 38. Bakker DJ. Ear-asymmetry with monaural stimulation: relations to lateral dominance and lateral awareness. Neuropsychologia 1970;8:103–117. 39. Fennell EB, Satz P, Morris R. The development of handedness and dichotic listening asymmetries in relation to school achievement: a longitudinal study. J Exp Child Psychol 1983;35:248–262.
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Rhinological and Otological Society, Inc.
Evidence for a Right Cochlear Implant Advantage in Simultaneous Bilateral Cochlear Implantation Yael Henkin, PhD; Riki Taitelbaum Swead, PhD; Daphne Ari-Even Roth, PhD; Liat Kishon-Rabin, PhD; Yisgav Shapira, MD; Lela Migirov, MD; Minka Hildesheimer, PhD; Ricky Kaplan-Neeman, PhD Objectives/Hypothesis: To compare speech perception performance with right versus left cochlear implants (CIs) in children with bilateral CIs implanted simultaneously. Study Design: Prospective case series of patients undergoing simultaneous bilateral cochlear implantation. Methods: Speech perception performance was tested in 10, right-handed children who received bilateral CIs simultaneously between 11 and 36 months (mean, 21 months), had at least 18 months of bilateral CI use, and were 5.3 years of age during testing. All children exhibited bilateral symmetrical severe-to-profound hearing loss prior to implantation and did not benefit from hearing aids. Speech perception performance was evaluated with the right CI and the left CI by means of an open-set monosyllabic word test in quiet presented at 45 dB HL in a sound field. Results: All children exhibited higher performance with the right CI compared to the left CI. Group mean performance with the right CI was 66.5% compared to 52% with the left CI (P 5.002), yielding a 14.5% difference. With increasing duration of bilateral CI use and age at evaluation, the right–left difference increased (r 5 0.72, P 5.019 and r 5 0.74, P 5.014, respectively). Conclusions: Current preliminary data indicate that children with bilateral CIs implanted simultaneously exhibit a significant right ear advantage for speech. Similarly to reports on normal-hearing children, right ear preference for speech increased with increasing age and auditory–linguistic experience. Thus, simultaneous bilateral cochlear implantation may lead to normal development of auditory pathways and may be an important contributor to the superior auditory, language, and communication skills reported in children with bilateral versus unilateral CIs. Key Words: Cochlear implant, bilateral simultaneous cochlear implantation, right ear advantage, speech perception, children. Level of Evidence: 4. Laryngoscope, 124:1937–1941, 2014
INTRODUCTION Over two decades of experience have shown that unilateral cochlear implants (CIs) substantially improve sound and speech perception thereby promoting development of speech, language, and communication skills.1–3 Despite these benefits, unilaterally implanted children are denied of the binaural advantages including summation, redundancy, squelch, and have limited access to interaural time and level differences. In addition, maximal benefit from the head shadow effect is restricted. From the Department of Communication Disorders (Y.H., D.A.-E.R., Sackler Faculy of Medicine, Tel Aviv University, Tel Aviv; and the Hearing, Speech, and Language Center (Y.H., R.T.S., D.A.-E.R., M.H., R.K.-N.), and Department of Otolaryngology–Head and Neck Surgery (Y.S., L.M.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel. Editor’s Note: This Manuscript was accepted for publication January 24, 2014. This work was performed at the Department of Communication Disorders, Sackler Faculy of Medicine, Tel Aviv University, and the Hearing, Speech, and Language Center, Sheba Medical Center, Tel Hashomer, Israel. The authors have no funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Yael Henkin, PhD, Department of Communication Disorders, Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel 52621. E-mail: [email protected] L.K.-R., M.H., R.K.-N.),
DOI: 10.1002/lary.24635
Laryngoscope 124: August 2014
Consequently, they exhibit difficulties in speech understanding in noise4 and sound localization5,6 and may show inferior expressive and receptive language skills7,8 compared to those of bilaterally implanted children and normal-hearing peers. In an attempt to diminish the negative effects of unilateral auditory deprivation and provide deaf children with binaural advantages, there is an increasing trend toward bilateral cochlear implantation. A recent worldwide survey indicated that 70% of bilateral implantations occur in children, with the highest representation of the 3- to 10-year-old age group (33% of all bilateral implantations), and children under 3 years (26%).9 In most cases, bilateral implants are provided sequentially, with variable periods between the first and second implantation. Nonetheless, there is growing agreement that “the infant or child with unambiguous cochlear implant candidacy should receive bilateral cochlear implants simultaneously as soon as possible after definitive diagnosis of deafness to permit optimal auditory development” (European Bilateral Pediatric Cochlear Implant Forum consensus statement).10 Although current guidelines have substantially reduced the minimal age at implantation, congenitally deaf children continue to experience various periods of bilateral and unilateral auditory deprivation prior to Henkin et al.: Right Ear Advantage and Bilateral CIs
1937
implantation, which may affect normal neurodevelopment and lead to reorganization of the central auditory system.11,12 In the normal auditory system, numerous functional imaging, electrophysiological, and behavioral studies have shown that although the auditory cortex receives sensory input from both ears, it is excited most strongly by stimulation of the contralateral ear.13–17 When stimulated by speech, stronger contralateral activation is manifested in the “right ear advantage” phenomenon using dichotic listening tasks, and is ascribed to stronger crossed auditory pathways from the right ear ascending to the speech-dominant left hemisphere.18 This asymmetry has been exhibited through the lifespan, from 4-day-old neonates19,20 to adulthood,21–25 to various speech stimuli (e.g., consonant–vowel syllables, stop consonants, and words).26–28 Recently published data indicate that unilateral cochlear implantation may alter the development of normal auditory pathways and result in cortical reorganization11,29; nevertheless, limited data exist regarding ear advantage patterns in unilateral CI recipients. Based on the well-substantiated right ear advantage for speech in normal-hearing listeners, it was speculated that the right ear should be the preferred ear for implantation30 in an attempt to maximize speech perception performance. This assertion has been tested in postlingually deafened adults and in prelingually deafened children, all implanted unilaterally. Data suggest that postlingually deafened elderly CI recipients implanted in the right ear outperformed those implanted in the left ear in speech perception tests in quiet (words) and in noise (sentences).31 Nonetheless, the right CI advantage was not evident in young postlingually deafened adults, with right versus left CI showing similar improvement on speech perception tests by 12 months of implant use.32 In prelingually deafened children, we reported data from a cohort of 71 children, 30 implanted in the right and 41 implanted in the left, indicating a slight yet significant right CI advantage that was evident throughout a 3-year follow-up and was independent of age at implantation.33 These results are in keeping with our earlier electrophysiological data showing differential brain activation patterns during speech processing in children with right versus left CI.34 Based on the recording of the P3 event-related potential known to reflect discrimination and categorization of stimuli, children implanted in the right ear exhibited bilateral temporal and frontal lobe activation while processing consonant–vowel syllables, similarly to normal-hearing controls. In contrast, children implanted in the left ear showed differential patterns characterized by enhanced ipsilateral temporal lobe activation. Following this line of investigation, we asked whether a right CI advantage for speech is evident in children with bilateral CI implanted simultaneously. The working premise was that children who experienced relatively short duration bilateral auditory deprivation and received simultaneous bilateral cochlear implants thereafter, may exhibit a right CI advantage for speech. For this purpose, we studied a group of children with bilateral CI who were implanted simultaneously, had substantial duration of CI use, and could fully cooperate in a speech perception test. Laryngoscope 124: August 2014
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MATERIALS AND METHODS Subjects Among the 497 children who were implanted at Sheba Medical Center, Tel Hashomer, between 1991 and 2013, 147 (30%) were implanted bilaterally. Of these, 48 received bilateral CIs simultaneously between 2007 and 2013, with the majority implanted between 2010 and 2013. Among the simultaneously implanted children, 10 children who were old enough to cooperate in speech perception testing and had at least 18 months of bilateral CI use participated in the study. They were implanted between 11 and 36 months of age (mean, 21.2 months) and used their CIs regularly for 18 to 75 months (mean, 44.2 months). Individual background information is presented in Table I. All children were diagnosed with bilateral severe-to-profound sensory neural hearing loss based on auditory brainstem response measurements and behavioral testing, and were habilitated bilaterally with high-power digital hearing aids shortly after diagnosis. They showed limited benefit from hearing aids as detailed in Table I. All were healthy, right-handed based on parental report, with fully inserted electrodes, and without cochlear malformations based on radiographic evaluation. All children were using oral communication and mainstreamed in regular educational settings. Seven children were congenitally deaf, whereas three children were deafened as a result of meningitis at 27, 33, and 20 months (Table I, subjects 1, 3, and 7, respectively). These three children were implanted 3, 4, and 6 months postmeningitis, respectively. Postoperative reports indicated complete cochlear ossification in the right ear and partial ossification in the left ear in patient 3, partial ossification in the basal turn especially in the right ear in patient 1, and no ossification in patient 7. The age at testing of all children ranged between 30 and 108 months (mean, 64.3 months). Seven children were implanted with MedEl devices, two with Cochlear devices, and one with Advanced Bionics devices. All electrodes were activated in all patients excluding three patients using MedEl devices: patient 3, electrode 12 bilaterally; patient 1, electrode 12 (left); patient 10, electrode 12 (right) and 11 (left).
Test Measures Speech perception was evaluated using the prerecorded Hebrew version of the Arthur Boothroyd (AB)35 open-set monosyllabic, consonant–vowel–consonant word recognition test. Based on clinical experience, the Hebrew AB test can be administered to young children. Two lists of AB words were presented in each of the two listening conditions, right CI and left CI, in random order. The words were presented at 45 dB HL in free field via two loudspeakers located at 45 on the right and left, at a distance of 1 m from the subject.
Statistical Methods The nonparametric Wilcoxon signed rank test was used to evaluate the difference in performance in the Hebrew AB test between the right and left CIs, as it was unlikely to be normally distributed. Furthermore, correlation between the right–left CI difference in performance and 1) age at implantation, 2) age at evaluation, and 3) duration of CI use, was evaluated by means of Pearson correlation coefficients.
RESULTS Aided thresholds, as measured by voice detection levels and speech reception thresholds with the right and left CIs, were comparable (P 5.25 and P 5.2, respectively) and are depicted in Figure 1. Henkin et al.: Right Ear Advantage and Bilateral CIs
TABLE I. Background Information of CI Recipients. Preimplantation ABR Thresholds to Clicks, 0.5, and 1 kHz Tone Bursts, dB nHL Patient
Etiology of Deafness
Aided VDL, dB HL*
Right
Left
Right
Left
Age at Implantation, mo
CI Devices
Duration of CI Use, mo
Age at Evaluation, mo
1
Meningitis
NR, NR, NR
NR, NR, NR
90
90
30
MedEl
75
105
2 3
Genetic Meningitis
NR, 90, NR NR, 80, NR
NR, NR,NR NR, 80, NR
45 55
40 55
12 36
MedEl MedEl
18 72
30 108
4
Unknown
NR, NR, NR
85, NR, NR
70
70
35
Cochlear
18
53
5 6
Genetic Genetic
NR, NR, NR NR, NR, NR
NR, NR, NR NR, NR, NR
60 100
70 100
15 12
MedEl Cochlear
48 18
63 30
7
Meningitis
NR, NR, NR
NR, NR, NR
75
55
26
MedEl
57
83
8 9
Connexin 26 Waardenburg
NR, NR, 100 NR, NR, NR
NR, NR, NR NR, NR, NR
30 80
55 60
11 13
MedEl Advanced Bionics
52 48
53 60
10
Genetic
NR, NR, NR
NR, NR, NR
90
90
22
MedEl
36
58
*Aided voice detection levels (VDL) in free field with hearing aids. ABR 5 auditory brainstem response; CI 5 cochlear implant; NR 5 no response at maximum output.
Figure 2 shows individual performance in the AB test with the right and left CIs and group mean data. For all participants, performance with the right CI was higher than with the left CI. Group mean performance was significantly higher with the right CI (66.5%) compared with the left CI (52%) (P 5.002) yielding a 14.5% difference. Three children who were deafened as a result of meningitis showed a larger right–left difference of 20%, 30%, and 20% (subjects 1, 3, and 7, respectively) compared to the seven prelingually deafened children who showed a mean difference of 10.7% (range, 5%–20%). Testing the right–left difference in the seven prelingually deafened children, yielded a significant right CI advantage (P 5.016).
Fig. 1. Group mean aided voice detection levels (VDL) and speech reception thresholds (SRT) with the right (Rt) and left (Lt) cochlear implants.
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The right–left difference in performance was strongly correlated with 1) age at evaluation (r 5 0.74, P 5.014) and 2) duration of implant use (r 5 0.72, P 5.019). These correlations are depicted in Figures 3 and 4 showing that with increasing age at evaluation and duration of CI use, the right–left difference increased. The correlation between the right–left difference and age at implantation was moderate yet did not reach significance (r 5 0.54, P 5.1).
DISCUSSION The current study provides first-time preliminary evidence indicating a significant right CI advantage of
Fig. 2. Individual and group mean speech perception performance with the right (Rt) and left (Lt) cochlear implants (CI).
Henkin et al.: Right Ear Advantage and Bilateral CIs
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Fig. 3. Right (Rt)–left (Lt) difference in performance as a function of age at evaluation. Note that with increasing age at evaluation, the right–left difference increases. CI 5 cochlear implant.
14.5% for speech in right-handed children with bilateral CIs implanted simultaneously at a young age. It is plausible that for this small group of children, all exhibiting a right CI advantage, simultaneous stimulation of auditory pathways resulted in the restoration of normal asymmetry. Support for this notion is provided by recent data collected by Gordon et al.11 showing that cortical activity, manifested by the P1 potential to biphasic electrical pulses in children who were implanted simultaneously or sequentially with short interimplant delay (2 years) showed a different pattern characterized by enhanced ipsilateral activation. Based on this finding, the authors concluded that bilateral auditory stimulation provided with limited delay can protect the brain from irreversible reorganization found in unilaterally implanted children or sequentially implanted children with long interimplant delay. Data regarding cortical activation patterns to speech stimuli are required to further clarify lateralization patterns to speech in CI recipients. The perceptual asymmetry found in the present study in CI recipients is not evident in normal-hearing listeners while performing monaural speech recognition tasks in quiet due to a ceiling effect. Typically, the right ear advantage is exhibited in normal-hearing listeners by means of dichotic listening tasks.25 Increased task difficulty and stimuli uncertainty, however, were also found to demonstrate this phenomenon.36 For example, competing monaural stimulation of words resulted in a substantial right ear advantage.37 For CI recipients, monaural speech recognition tasks with low linguistic redundancy (i.e., monosyllabic words), even in quiet, are challenging and may therefore suffice to demonstrate the CI side advantage. Support for this notion is the remarkably similar magnitude of the right CI advantage found in children with bilateral CI implanted simultaneously in the current study (14.5%) and that found in Laryngoscope 124: August 2014
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unilaterally implanted recipients with right versus left CI while performing a monosyllabic word test in quiet (children: 13.7%33, elderly adults: approximately 13%31). It should further be noted that the right CI advantage was persistent over 2 and 3 years of follow-up in children and in elderly adults, as reported by Henkin et al.33 and Budenz et al.,31 respectively. Increased contralateral lateralization of cortical activity (during the P1 potential) toward the linguistically dominant left hemisphere in children with unilateral right CI,11 together with data showing similar bilateral activation (during the P3 potential) to speech sounds in children with right CI and normal-hearing peers,34 may elucidate the differences in performance between children with a right and left CI.33 Interestingly, the right CI advantage was more prominent in three perilingually deafened children who suffered meningitis at 20, 27, and 33 months and were implanted shortly thereafter (3–6 months), compared to the remaining seven children who were all prelingually deafened and implanted at a mean age of 17 months. The meaning of the magnitude of the right CI advantage in a monaural speech perception task in quiet is unclear. Nonetheless, the more pronounced right–left difference in the perilingual children (23%) compared to the prelingual children (11%) may reflect substantial time in sound and exposure to language prior to loss of hearing, together with their older age at evaluation. For the currently studied group, the duration of CI use and age at evaluation were strongly correlated with the right–left difference. In other words, with increasing duration of implant use from 18 to 75 months and increasing age at evaluation from 30 to 108 months, the right CI preference increased. This finding is in agreement with dichotic listening data from normal-hearing right-handed children showing that the right ear preference for verbal material increased with age from 7 to 13 years.37,38 It has been suggested that developmental increases in attention, working memory, and language skills may enlarge the magnitude of ear advantage.25,39
Fig. 4. Right (Rt)–left (Lt) difference in performance as a function of duration of bilateral cochlear implant (CI) use. Note that with increasing duration of bilateral CI use, the right–left difference increases.
Henkin et al.: Right Ear Advantage and Bilateral CIs
Finally, recent data from a multicenter study show superior expressive and receptive language skills in 25 children with bilateral CI compared to carefully matched children with unilateral CI after 3 years of CI use. Moreover, eight children who were implanted simultaneously achieved higher expressive word development scores compared to those who were implanted sequentially. It is reasonable to assume that improved sound localization and speech perception in quiet and in challenging listening environments reported for children with bilateral CI facilitates incidental learning that is crucial for normal language development. Moreover, it is plausible that simultaneous bilateral cochlear implantation led to normal development of auditory pathways and restored the right ear advantage for speech that is typical in the presence of normal hearing.
CONCLUSION Current preliminary data indicate that children with bilateral CIs implanted simultaneously exhibited a significant right ear advantage for speech presented monaurally in quiet. Similarly to reports on normal-hearing children, right ear preference for speech increased with increasing age and auditory–linguistic experience. Thus, simultaneous bilateral cochlear implantation may lead to normal development of auditory pathways and may be an important contributor to the superior auditory, language, and communication skills reported in children with bilateral versus unilateral CI.
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