Eur Arch Otorhinolaryngol DOI 10.1007/s00405-014-3319-5
OTOLOGY
Speech and language development after cochlear implantation in children with bony labyrinth malformations: long-term results Tolgahan Catli • Burcu Uckan • Levent Olgun
Received: 19 July 2014 / Accepted: 30 September 2014 Ó Springer-Verlag Berlin Heidelberg 2014
Abstract The aim of this study was to investigate speech and language development after long-term cochlear implantation in children with bony labyrinth malformations (BLMs) and to present the surgical findings in this group of patients. The auditory and linguistic skills of 21 children who had BLM were assessed in this study. They were implanted between 1998 and 2009. Twenty-two sex-matched and age-matched implantees without BLM were evaluated as the control group. To compare speech perception and speech intelligibility between the groups, the categories of auditory performance (CAP) test and speech intelligibility rating (SIR) test, respectively, were administered. The Turkish version of the Test of Early Language Development (TELD-3-T) was administered to evaluate and compare the linguistic skills of the groups. Surgical findings and complications were also analyzed. Implanted anomalies were common cavity in five patients, incomplete partition type 1 in 5 patients, and incomplete partition type 2 in 11 patients. The CAP and SIR scores were significantly higher in the control group (p \ 0.05), but the TELD-3-T test scores were comparable among the groups (p [ 0.05). Based on the specific type of malformation, the CAP and SIR scores were comparable between the subgroups (p [ 0.05). No perioperative complications occurred in the control group. However, various perioperative complications (gusher, etc.) and surgical difficulty T. Catli (&) L. Olgun Department of Otorhinolaryngology, Bozyaka Teaching and Research Hospital, Saim Cikrikci Street, 35320 Bozyaka, Izmir, Turkey e-mail: [email protected] B. Uckan Department of Otorhinolaryngology, Medikar Hospital, Karabuk, Turkey
occurred in the anomaly group. The malformation group had unsatisfactory results with regard to speech perception skills; however, this group and the non-anomalous group exhibited comparable long-term results on linguistic development. Keywords Bony labyrinth malformation Cochlear implantation Language development Speech intelligibility Speech perception
Introduction Since the first artificial stimulation of the auditory apparatus by Parisian scientists Djourno and Eyries [1], cochlear implant technology has considerably improved. It appears to be the best way to rehabilitate patients who have severe to profound sensorineural hearing loss with an intact cochlear nerve and central auditory pathway. This procedure has a crucial role in speech and language development in these groups of patients and continues to improve with technological advancements [2]. In the beginning of the cochlear implantation (CI) era, any type of inner ear malformation was considered a contraindication for the procedure. However, in the early 1980s, Brazilian otologist Mangabeira-Albernaz [3] reported the first known implanted patient with an anomalous inner ear without complications. Malformations of the bony labyrinth represent approximately 20 % of cases of congenital sensorineural hearing loss [4]. Many authors have defined various types of these malformations. Jackler et al. [4] proposed a classification of bony labyrinth malformations that is based on radiological and audiological findings. Sennaroglu and Saatci suggested a new classification based primarily on radiological findings for incomplete partition (IP) of the
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cochleovestibular system: IP type 1 (IP-1: the cochlea is lacking the entire modiolus and cribriform area, resulting in a cystic appearance. This is accompanied by a large cystic vestibule) and IP type 2 (IP-2: Mondini deformity: the cochlea consists of 1.5 turns, in which the middle and apical turns coalesce to form a cystic apex, accompanied by a dilated vestibule and enlarged VA) [5]. Common cavity (CC) corresponds to a sole cystic cavity, represents both the cochlea and the vestibule, with no evidence of differentiation into cochlea and vestibule (Fig. 1). Sennaroglu [6] also updated his classification and added a third type of IP, which is characterized with X-linked deafness. To date, electron microscope studies and radiologic studies have identified different structural and histological properties of malformations [5, 7]. These structural malformations are the major reasons for concerns in the CI procedure in this group of patients. In the present study, we aimed to assess the speech and language development after CI in implantees with bony labyrinth malformations (BLMs). Existing studies have predominantly investigated this topic and have presented the early results. However, our aim was to investigate the long-term results. We also share our surgical findings to discuss the surgical difficulties and complications of the procedure.
Materials and methods Ethical committee of the institution approved the study protocol and informed consent was obtained from all participants. Twenty-one patients with BLM and 22 patients without BLM (i.e., normal bony labyrinths) were recruited as the study group and control group, respectively. All study patients were classified in accordance with the Sennaroglu and Saatci classification system [6]. Patients with Michel aplasia, cochlear agenesis, severe cochlear
hypoplasia, and cochlear nerve agenesis were excluded from the study. In addition, three patients with unilateral BLM were also excluded. Furthermore, patients with mental retardation and autism were excluded from the study, even if they had undergone an uncomplicated surgical procedure. Twenty-two patients with an isolated large vestibular aqueduct were excluded because they had highly successful audiological and surgical results. Speech perception, speech intelligibility, and language development of the implanted children in both groups were evaluated with the categories of auditory performance (CAP) test, speech intelligibility rating (SIR) test, and the Turkish Test of Early Language Development (TELD-3-T) test. All tests were conducted in a quiet room using a live voice presented at approximately the 70 dB sound pressure level. Speech perception was measured using the CAP score. The CAP is a nonlinear hierarchical scale used to rate a child’s developing auditory abilities [8]. It uses the eight categories presented in Table 1. Speech intelligibility was measured by the SIR scores presented in Table 2. The SIR test was designed as a time-effective global outcome measure of speech production in daily life circumstances [9]. The tests were performed by the same team at our institution. Language development was assessed using the TELD-3-T test battery. The TELD-3-T test is an adaptation of the English version of the Test of Early Language Development (3rd edition), which assesses receptive
Table 1 The capacity of auditory performance (CAP) 0
No awareness of environmental sounds
1
Awareness of environmental sounds
2
Response to speech sounds
3
Identification of environmental sounds
4
Discrimination of some speech sounds without lipreading
5
Understanding of common phrases without lipreading
6
Understanding of conversation without lipreading
7
Use of telephone with known listener
Table 2 Speech intelligibility rating (SIR)
Fig. 1 Common cavity deformity (patient number 18)
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Category 1
Connected speech is unintelligible. Pre-recognizable words in spoken language, primary mode of communication may be manual
Category 2
Connected speech is unintelligible. Intelligible speech is developing in single words when context and lipreading cues are available
Category 3
Connected speech is intelligible to a listener who concentrates and lipreads
Category 4
Connected speech is intelligible to a listener who has little experience of a deaf person’s speech
Category 5
Connected speech is intelligible to all listeners. Child is understood easily in everyday contexts
Eur Arch Otorhinolaryngol
language and expressive language in children [10, 11]. Both tests have two forms, which contain receptive and expressive language subtests. TELD-3-T is administered in the following way. Test begins at the entry point for each implantee, which is based on their age. To specify their basal point in the test, implantees are expected to answer three consecutive items correctly. If a child does not succeed in three items in a row, testing continues backwards until this is met. The threshold is determined when the child makes three mistakes in a row. Perioperative findings and related complications were recorded and evaluated. Data analysis and statistical processing Statistical analysis of the data was conducted with SPSS 21.0.0 (SPSS Inc.S, Chicago, IL, USA). The results of each group were compared using Mann–Whitney U test. Kruskal–Wallis test was used compare the results of BLM subgroups. A ‘‘p’’ value \0.05 was considered significant.
Results Since 1998 in our clinic, 1,673 pediatric and adult patients with severe to profound hearing loss have been rehabilitated via CI. Between 1998 and 2009, 816 of these patients were implanted. Five hundred eighty-one of the 816 patients were children, and 33 of these children had BLM (representing 1.9 % of all patients implanted between 1998 and 2009). Twenty-one patients (11 females and 10 males) of the 33 patients had bilateral BLM and were recruited as the study group. These malformations were as follows; common cavity in 5 patients, incomplete partition type 1 (IP-1) in 5 patients, and incomplete partition type 2 (IP-2) in 11 patients. To establish a control group, 22 age-matched and sex-matched implantees (12 females, 10 males) with normal bony labyrinths were chosen. The etiologies of hearing losses in children with BLM and control group were: congenital rubella in 2, Waardenburg syndrome in 3, hereditary in 4, idiopathic in 12 patients and prematurity in 1, Waardenburg syndrome in 3, hereditary in 5, idiopathic in 13 patients, respectively. The age at implantation ranged 20–74 months (median age 44.72 months) in the study group and ranged 19–73 months (median age 42.68 months) in the control group. The difference was statistically insignificant (p [ 0.05). The length of hearing aid use before implantation was 7–30 months (median time 15.08 months) and 7–25 months (median time 14.81 months) in the study group and control group, respectively. The difference was statistically insignificant (p [ 0.05). All patients in both groups have been implanted unilaterally. Both implanted and un-implanted (contralateral) ears of the patients had profound sensorineural
hearing loss. All patients in study and control group were not using hearing aid in contralateral ears postoperatively. In total, 42 ears of 21 patients with BLM were classified according to the Sennaroglu and Saatci classification system, as follows: two ears had Michel deformity, nine ears had a common cavity (CC), eight ears had IP-1, and 23 ears had IP-2. The implantation age of the patients and the length of hearing aid usage ranged 19–73 months (median time 42.68 months) and 7–25 months (median time 12.81 months), respectively, for the BLM group, and ranged 20–74 months (median time 44.72 months) and 7–30 months (median time 16.08), respectively, for the control group. The BLM group was implanted with the MED-EL (MED-EL Corp., Austria) Combi 40? implant in six patients, the MED-EL Pulsar implant in ten patients, the Clarion I (Advanced Bionics Corp., USA) implant in one patient, the Clarion II implant in one patient, the Clarion HiRes 90K implant in two patients, and the Nucleus Freedom (Cochlear Corp., Australia) Contour Advance in one patient. The control group was implanted with the MED-EL Combi 40? implant in 11 patients, the MED-EL Pulsar implant in 16 patients, the Clarion I implant in one patient, the Clarion II implant in two patients, the Clarion HiRes 90K implant in four patients, the Nucleus Freedom Contour Advance implant in two patients, and the Nucleus 24 Contour Advance implant in one patient. Surgical findings The senior author of this study and the same surgical team performed the surgical procedures. Perioperative findings were described as the presence of a cerebrospinal fluid (CSF) gusher, abnormality of the facial nerve, or other malformation around the temporal bone. Electrode insertion was performed via cochleostomy in 19 patients, by posterior labyrinthotomy in one patient, and by the round window in two patients. A perioperative CSF gusher occurred in 14 of 21 patients in the BLM group. Except for CC, all five IP-1 patients and nine IP-2 patients developed a gusher during the procedure. The cochleostomy was sealed with fat tissue and fibrin glue. The patient’s head was elevated postoperatively to manage the gusher. Except in two IP-1 patients, the gusher stopped with these interventions. For these two intractable cases, revision surgery was performed on the second postoperative day in one patient and in the third month in the other patient. Four patients had an anteriorly and laterally displaced facial nerve, which made the procedure risky. For this reason, cochleostomy could not be performed via a facial recess approach in two patients with CC and an abnormal facial nerve course. Therefore, the procedure was performed by the transcanal approach. In addition, in one patient with Klippel–Feil syndrome with neck anomaly and in another patient with a superiorly
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displaced cochlea, cochleostomy could not be performed via posterior tympanotomy. Their cochleostomies were performed via transcanal approach. In one patient who had IP-2, the fitting was unsatisfactory because of the vestibular displacement of the electrodes. This was diagnosed after the radiologic evaluation. This patient was again explored surgically and the electrode was correctly placed so that electrical stimulation was maintained adequately. On assessing commonly known late-type complications, we did not experience long-term complications in our BLM patients such as a late gusher or meningitis. Timing of the tests Speech and language development tests were performed for a median of 91 months (range 40–129 months) in the BLM group and for 96 months (range 42–139 months) in the control group. The difference was not statistically significant (p [ 0.05).
(range 4–7) in the control group and 5 (range 5–7) in the BLM group; the median SIR score was 4.5 (range 2–5) in the control group and 3 (range 2–5) in the BLM group) (p = 0.002 for CAP, p = 0.007 for SIR). The analysis of the speech perception test results, based on the specific type of malformation, showed that the both CAP and SIR scores were comparable between the IP-2, IP-1 and CC groups (p [ 0.05) (Table 3). Language development results The median receptive language development test score of the anomaly group was 22 (range 8–36) while median receptive language development test score of the control group was 27 (range 10–34) (p [ 0.05). Besides, the median expressive language development test score of the anomaly group was 22 (range 11–38) while median expressive language development test score of the control group was 28 (range 13–39) (p [ 0.05).
Speech perception and intelligibility results Discussion A comparison of the results of the CAP scores and SIR scores between the groups revealed that the scores in both test batteries were significantly higher in the control group than in the BLM group (the median CAP score was 7 Table 3 Patient details of the BLM group
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During the first years of the CI era, anomalous cochleae were a big problem for the neuro-otologists and there were several issues in performing the procedure. The first issue
Patient number
Type of BLM on implanted side
Type of CI
SIR score (category)
CAP score
1
IP-2
MED-EL Pulsar
2
5
2
IP-1
Clarion HiRes 90K
2
4
3 4
IP-2 IP-2
Clarion II MED-EL Pulsar
4 5
5 7
5
CC
MED-EL Pulsar
2
5
6
IP-2
MED-EL Pulsar
4
4
7
CC
MED-EL (Combi 40?)
3
4
8
IP-1
Clarion HiRes 90K
2
4
9
IP-2
Clarion I
2
3
10
CC
MED-EL Pulsar
3
6
11
IP-2
MED-EL Pulsar
5
7
12
CC
MED-EL (Combi 40?)
3
6
13
IP-2
MED-EL Pulsar
4
6
14
IP-2
MED-EL (Combi 40?)
5
7
15
IP-1
MED-EL Pulsar
3
5
16
IP-1
MED-EL Pulsar
3
5
17
IP-1
MED-EL Pulsar
4
6
18
CC
MED-EL (Combi 40?)
2
4
19 20
IP-2 IP-2
MED-EL (Combi 40?) Nucleus Freedom Contour Advance
4 5
6 7
21
IP-2
MED-EL (Combi 40?)
2
5
Eur Arch Otorhinolaryngol
was related to anatomical difficulties that make the procedure more challenging. The second issue concerned the sufficiency of the electrical stimulation of the cochlear neural structures provided by the cochlear implant. The third issue concerned the development of the auditory and linguistic skills of these groups of children after the operation. These issues are less problematic these days, although they still exist to varying degrees. For instance, our findings revealed that these groups of patients were more prone to surgical complications. The major challenge is the risk of having a CSF ‘‘gusher’’ occur intraoperatively. In particular, the IP-1 patients had a high incidence of experiencing a real ‘‘gusher’’ (i.e., not oozing) because of the large defect between the internal auditory canal and the malformed cochlea. However, other types of malformations are more prone to developing a gusher, compared to normal inner ears. In our series, a gusher occurred in all (100 %) of the 5 IP-1 patients, 9 (82 %) of 11 IP-2 patients, and 0 (0 %) of 5 CC patients. This indicates that 66.6 % (14 patients) of the 21 BLM patients had a gusher in our series. In other series, the approximate rate varies for a gusher occurring during the implantation of patients with a malformed inner ear. For example Hoffman et al. [12] found that 40 % of patients with BLM had a CSF gusher, regardless of the type of the malformation. Most reports reveal that the incidence of a gusher occurs in 40–50 % of patients with BLM [6]. Wootten et al. [13] reported the lowest percentage (1 %) of gushers in their patients. According to Papsin [14], the different percentages in the rate of gusher originated from the definition of the gusher. Papsin says the term ‘‘gusher’’ should be used only to describe the pulsatile outflow of the fluid and that minor egresses should not be described as a gusher. That is the source of the high incidences of gusher. In our opinion, our patients fulfill the gusher criteria and our rate is higher than most published rates. Another problem during the surgery of patients with BLM is the malpositioned facial nerve. As we noted in our series, four patients had an anteriorly and laterally displaced facial nerve, which made the procedure risky. For this reason, a cochleostomy could not be performed via facial recess approach in two patients with a CC and malpositioned facial nerve. They required a combined transcanal approach. In the literature, various reports indicate variability in the course of the facial nerve in patients with BLM [15–17]. Luntz et al. [18] and Khalessi et al. [19] reported patients with CC and a malpositioned facial nerve. Similar to Luntz and Khalessi, our two patients had a CC and we used a transcanal approach to perform a safe cochleostomy. An abnormal course of the facial nerve makes it more prone to surgical trauma, as Hoffman et al. [12] experienced with his patient. To secure the facial nerve during the procedure, some authors
recommend intraoperative monitoring of the nerve [6]. In our practice we do not use facial monitoring. Other important aspects of the implantation procedure for patients with BLM are (1) the cochlear implant provides sufficient electrical stimulation of the cochlear neural structures and (2) the development of the auditory and linguistic skills of these groups of children after the operation. In their study, Blamey et al. [20] state that at least 5,000 ganglion cells are required to achieve satisfactory speech perception after patients undergo CI. These statements and findings give hope because Schmidt [21] in a histological study found 7,677 cochlear neurons in a patient with Mondini dysplasia. From the histological level to the clinical end point (and paralleling the histological findings), various clinical studies demonstrate that patients with BLM who received CI can achieve audiological results comparable to those of patients who have a normal cochlear structure [17, 18]. In contrast to these histological and audiological findings, our results demonstrated that patients with BLM could not achieve results after CI that were comparable to those of patients who had a normal bony labyrinth with regard to speech perception (based on the CAP test) and speech intelligibility (based on the SIR tests). However, on analyzing the results based on the specific type of BLM, we showed that both the CAP and SIR scores were comparable between the specific type of malformations (IP-1, IP-2 and CC). In contrast to our findings about specific type of malformations, Mylanus et al. [22] conclude that severe malformations lead to poorer performances regarding speech perception tests. Actually the follow-up period of the patients in our study is longer than other studies in the literature. Different results regarding speech perception and intelligibility may attribute to different follow-up periods and also to the different number of patients (21 and 13 patients in our and Mylanus study, respectively). Our results concerning language development are comparable among the groups and indicate that patients who have BLM can achieve satisfactory results in the development of their linguistic skills that are comparable to the results of patients with normal bony labyrinths. Many authors have investigated the language development of patients after CI, although the authors focused on implantees with normal bony labyrinths [23, 24]. They showed that children could achieve satisfactory language development after CI. However, as Lee et al. [25] state, having an additional handicap such as mental retardation can have a negative impact on achieving satisfactory language development. We did not include any patient with mental retardation in our study group. In contrast to the speech development results, achieving comparable results in language development tests between the groups may indicate that it is not a substantial problem
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for implantees who have BLM to perform linguistic skills successfully after the CI procedure. Malformations such as IP or CC, based on their disordered cochlear structures, may diminish cochlear neuronal excitability or peripheral hearing; however, other skills such as language development could possibly survive because of their more complicated developmental process. We believe that proper assistance after implantation—especially audiological and linguistic rehabilitation administered by the audiology team and family support—could result in satisfactory linguistic skills.
8.
9.
10. 11. 12.
13.
Conclusion 14.
The data presented in this paper indicate that the CI procedure in children with BLM has some difficulties related to the surgical procedure and audiological outcomes. Peripheral hearing performances are significantly lower for patients with a BLM, although these patients and patients who have a normal bony labyrinth may improve their communication ability. Conflict of interest interest.
Authors declare that there is no competing
15.
16.
17.
18.
19.
References 1. Eisen MD (2003) Djourno, Eyries, and the first implanted electrical neural stimulator to restore hearing. Otol Neurotol 24:500–506 2. Dettman SJ, Fikret H, Dowell RC, Charlton M, Williams SS, Tomov AM, Barker EJ (2004) Speech perception results for children using cochlear implants who have additional special needs. Volta Rev 104:361–392 3. Mangabeira-Albernaz PL (1983) The Mondini dysplasia: from early diagnosis to cochlear implant. Acta Otolaryngol 95:627–631 4. Jackler RK, Luxford WM, House WF (1987) Congenital malformations of the inner ear: a classification based on embryogenesis. Laryngoscope 97:2–14 5. Sennaroglu L, Saatci I (2002) A new classification for cochleovestibular malformations. Laryngoscope 112:2230–2241 6. Sennaroglu L (2010) Cochlear implantation in inner ear malformations—a review article. Cochlear Implants Int 11:4–41 7. Sainz M, Garcia-Valdecasas J, Fernandez E, Pascual MT (2012) Auditory maturity and hearing performance in inner ear
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malformations: a histological and electrical stimulation approach. Eur Arch Otorhinolaryngol 269:1583–1587 Archbold S, Lutman M, Marchall D (1995) Categories of auditory performance. Ann Otol Rhinol Laryngol 166(Suppl 104):312–314 Allen C, Nikolopoulos TP, Dyar D, O’Donoghue GM (2001) Reliability of a rating scale for measuring speech intelligibility after pediatric cochlear implantation. Otol Neurotol 22:631–633 Hresko WP, Reid DK, Hammill DD (1999) Test of early language development, 3rd edn. Pro-ed, Austin Topbas¸ S, Gu¨ven S (2007) Test of Early Language Development (TELD-3): Turkish version. Anadolu University, Eskis¸ ehir Hoffman RA, Downey LL, Waltzman SB, Cohen NL (1997) Cochlear implantation in children with cochlear malformations. Am J Otol 18:184–187 Wootten CT, Backous DD, Haynes DS (2006) Management of cerebrospinal fluid leakage from cochleostomy during cochlear implant surgery. Laryngoscope 116:2055–2059 Papsin BC (2005) Cochlear implantation in children with anomalous cochleovestibular anatomy. Laryngoscope 115:1–26 Molter DW, Pate BR Jr, McElveen JT Jr (1993) Cochlear implantation in the congenitally malformed ear. Otolaryngol Head Neck Surg 108:174–177 Kim LS, Jeong SW, Huh MJ, Park YD (2006) Cochlear implantation in children with inner ear malformations. Ann Otol Rhinol Laryngol 115:205–214 Eisenman DJ, Ashbaugh C, Zwollan TA, Arts HA, Telian SA (2001) Implantation of the malformed cochlea. Otol Neurotol 22:834–841 Luntz M, Balkany T, Hodges A, Telischi FF (1997) Cochlear implants in children with congenital inner ear malformations. Arch Otolaryngol Head Neck Surg 123:974–977 Khalessi MH, Zarandi MM, Borghei P, Abdi S (2004) Cochlear implantation in patients with inner ear malformations. Acta Med Iran 42:188–197 Blamey P (1997) Are spiral ganglion cell numbers important for speech perception with a cochlear implant? Am J Otol 18(Suppl 6):S11–S12 Schmidt JM (1985) Cochlear neuronal populations in developmental defects of the inner ear. Implications for cochlear implantation. Acta Otolaryngol 99:14–20 Mylanus EAM, Rotteveel LJC, Leeuw RL (2004) Congenital malformation of the inner ear and pediatric cochlear implantation. Otol Neurotol 25:308–317 May-Mederake B (2012) Early intervention and assessment of speech and language development in young children with cochlear implants. Int J Pediatr Otorhinolaryngol 76:939–946 Geers AE (2006) Factors influencing spoken language outcomes in children following early cochlear implantation. Adv Otorhinolaryngol 64:50–65 Lee YM, Kim LS, Jeong SW, Kim JS, Chung SH (2010) Performance of children with mental retardation after cochlear implantation: speech perception, speech intelligibility, and language development. Acta Otolaryngol 130:924–934
OTOLOGY
Speech and language development after cochlear implantation in children with bony labyrinth malformations: long-term results Tolgahan Catli • Burcu Uckan • Levent Olgun
Received: 19 July 2014 / Accepted: 30 September 2014 Ó Springer-Verlag Berlin Heidelberg 2014
Abstract The aim of this study was to investigate speech and language development after long-term cochlear implantation in children with bony labyrinth malformations (BLMs) and to present the surgical findings in this group of patients. The auditory and linguistic skills of 21 children who had BLM were assessed in this study. They were implanted between 1998 and 2009. Twenty-two sex-matched and age-matched implantees without BLM were evaluated as the control group. To compare speech perception and speech intelligibility between the groups, the categories of auditory performance (CAP) test and speech intelligibility rating (SIR) test, respectively, were administered. The Turkish version of the Test of Early Language Development (TELD-3-T) was administered to evaluate and compare the linguistic skills of the groups. Surgical findings and complications were also analyzed. Implanted anomalies were common cavity in five patients, incomplete partition type 1 in 5 patients, and incomplete partition type 2 in 11 patients. The CAP and SIR scores were significantly higher in the control group (p \ 0.05), but the TELD-3-T test scores were comparable among the groups (p [ 0.05). Based on the specific type of malformation, the CAP and SIR scores were comparable between the subgroups (p [ 0.05). No perioperative complications occurred in the control group. However, various perioperative complications (gusher, etc.) and surgical difficulty T. Catli (&) L. Olgun Department of Otorhinolaryngology, Bozyaka Teaching and Research Hospital, Saim Cikrikci Street, 35320 Bozyaka, Izmir, Turkey e-mail: [email protected] B. Uckan Department of Otorhinolaryngology, Medikar Hospital, Karabuk, Turkey
occurred in the anomaly group. The malformation group had unsatisfactory results with regard to speech perception skills; however, this group and the non-anomalous group exhibited comparable long-term results on linguistic development. Keywords Bony labyrinth malformation Cochlear implantation Language development Speech intelligibility Speech perception
Introduction Since the first artificial stimulation of the auditory apparatus by Parisian scientists Djourno and Eyries [1], cochlear implant technology has considerably improved. It appears to be the best way to rehabilitate patients who have severe to profound sensorineural hearing loss with an intact cochlear nerve and central auditory pathway. This procedure has a crucial role in speech and language development in these groups of patients and continues to improve with technological advancements [2]. In the beginning of the cochlear implantation (CI) era, any type of inner ear malformation was considered a contraindication for the procedure. However, in the early 1980s, Brazilian otologist Mangabeira-Albernaz [3] reported the first known implanted patient with an anomalous inner ear without complications. Malformations of the bony labyrinth represent approximately 20 % of cases of congenital sensorineural hearing loss [4]. Many authors have defined various types of these malformations. Jackler et al. [4] proposed a classification of bony labyrinth malformations that is based on radiological and audiological findings. Sennaroglu and Saatci suggested a new classification based primarily on radiological findings for incomplete partition (IP) of the
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cochleovestibular system: IP type 1 (IP-1: the cochlea is lacking the entire modiolus and cribriform area, resulting in a cystic appearance. This is accompanied by a large cystic vestibule) and IP type 2 (IP-2: Mondini deformity: the cochlea consists of 1.5 turns, in which the middle and apical turns coalesce to form a cystic apex, accompanied by a dilated vestibule and enlarged VA) [5]. Common cavity (CC) corresponds to a sole cystic cavity, represents both the cochlea and the vestibule, with no evidence of differentiation into cochlea and vestibule (Fig. 1). Sennaroglu [6] also updated his classification and added a third type of IP, which is characterized with X-linked deafness. To date, electron microscope studies and radiologic studies have identified different structural and histological properties of malformations [5, 7]. These structural malformations are the major reasons for concerns in the CI procedure in this group of patients. In the present study, we aimed to assess the speech and language development after CI in implantees with bony labyrinth malformations (BLMs). Existing studies have predominantly investigated this topic and have presented the early results. However, our aim was to investigate the long-term results. We also share our surgical findings to discuss the surgical difficulties and complications of the procedure.
Materials and methods Ethical committee of the institution approved the study protocol and informed consent was obtained from all participants. Twenty-one patients with BLM and 22 patients without BLM (i.e., normal bony labyrinths) were recruited as the study group and control group, respectively. All study patients were classified in accordance with the Sennaroglu and Saatci classification system [6]. Patients with Michel aplasia, cochlear agenesis, severe cochlear
hypoplasia, and cochlear nerve agenesis were excluded from the study. In addition, three patients with unilateral BLM were also excluded. Furthermore, patients with mental retardation and autism were excluded from the study, even if they had undergone an uncomplicated surgical procedure. Twenty-two patients with an isolated large vestibular aqueduct were excluded because they had highly successful audiological and surgical results. Speech perception, speech intelligibility, and language development of the implanted children in both groups were evaluated with the categories of auditory performance (CAP) test, speech intelligibility rating (SIR) test, and the Turkish Test of Early Language Development (TELD-3-T) test. All tests were conducted in a quiet room using a live voice presented at approximately the 70 dB sound pressure level. Speech perception was measured using the CAP score. The CAP is a nonlinear hierarchical scale used to rate a child’s developing auditory abilities [8]. It uses the eight categories presented in Table 1. Speech intelligibility was measured by the SIR scores presented in Table 2. The SIR test was designed as a time-effective global outcome measure of speech production in daily life circumstances [9]. The tests were performed by the same team at our institution. Language development was assessed using the TELD-3-T test battery. The TELD-3-T test is an adaptation of the English version of the Test of Early Language Development (3rd edition), which assesses receptive
Table 1 The capacity of auditory performance (CAP) 0
No awareness of environmental sounds
1
Awareness of environmental sounds
2
Response to speech sounds
3
Identification of environmental sounds
4
Discrimination of some speech sounds without lipreading
5
Understanding of common phrases without lipreading
6
Understanding of conversation without lipreading
7
Use of telephone with known listener
Table 2 Speech intelligibility rating (SIR)
Fig. 1 Common cavity deformity (patient number 18)
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Category 1
Connected speech is unintelligible. Pre-recognizable words in spoken language, primary mode of communication may be manual
Category 2
Connected speech is unintelligible. Intelligible speech is developing in single words when context and lipreading cues are available
Category 3
Connected speech is intelligible to a listener who concentrates and lipreads
Category 4
Connected speech is intelligible to a listener who has little experience of a deaf person’s speech
Category 5
Connected speech is intelligible to all listeners. Child is understood easily in everyday contexts
Eur Arch Otorhinolaryngol
language and expressive language in children [10, 11]. Both tests have two forms, which contain receptive and expressive language subtests. TELD-3-T is administered in the following way. Test begins at the entry point for each implantee, which is based on their age. To specify their basal point in the test, implantees are expected to answer three consecutive items correctly. If a child does not succeed in three items in a row, testing continues backwards until this is met. The threshold is determined when the child makes three mistakes in a row. Perioperative findings and related complications were recorded and evaluated. Data analysis and statistical processing Statistical analysis of the data was conducted with SPSS 21.0.0 (SPSS Inc.S, Chicago, IL, USA). The results of each group were compared using Mann–Whitney U test. Kruskal–Wallis test was used compare the results of BLM subgroups. A ‘‘p’’ value \0.05 was considered significant.
Results Since 1998 in our clinic, 1,673 pediatric and adult patients with severe to profound hearing loss have been rehabilitated via CI. Between 1998 and 2009, 816 of these patients were implanted. Five hundred eighty-one of the 816 patients were children, and 33 of these children had BLM (representing 1.9 % of all patients implanted between 1998 and 2009). Twenty-one patients (11 females and 10 males) of the 33 patients had bilateral BLM and were recruited as the study group. These malformations were as follows; common cavity in 5 patients, incomplete partition type 1 (IP-1) in 5 patients, and incomplete partition type 2 (IP-2) in 11 patients. To establish a control group, 22 age-matched and sex-matched implantees (12 females, 10 males) with normal bony labyrinths were chosen. The etiologies of hearing losses in children with BLM and control group were: congenital rubella in 2, Waardenburg syndrome in 3, hereditary in 4, idiopathic in 12 patients and prematurity in 1, Waardenburg syndrome in 3, hereditary in 5, idiopathic in 13 patients, respectively. The age at implantation ranged 20–74 months (median age 44.72 months) in the study group and ranged 19–73 months (median age 42.68 months) in the control group. The difference was statistically insignificant (p [ 0.05). The length of hearing aid use before implantation was 7–30 months (median time 15.08 months) and 7–25 months (median time 14.81 months) in the study group and control group, respectively. The difference was statistically insignificant (p [ 0.05). All patients in both groups have been implanted unilaterally. Both implanted and un-implanted (contralateral) ears of the patients had profound sensorineural
hearing loss. All patients in study and control group were not using hearing aid in contralateral ears postoperatively. In total, 42 ears of 21 patients with BLM were classified according to the Sennaroglu and Saatci classification system, as follows: two ears had Michel deformity, nine ears had a common cavity (CC), eight ears had IP-1, and 23 ears had IP-2. The implantation age of the patients and the length of hearing aid usage ranged 19–73 months (median time 42.68 months) and 7–25 months (median time 12.81 months), respectively, for the BLM group, and ranged 20–74 months (median time 44.72 months) and 7–30 months (median time 16.08), respectively, for the control group. The BLM group was implanted with the MED-EL (MED-EL Corp., Austria) Combi 40? implant in six patients, the MED-EL Pulsar implant in ten patients, the Clarion I (Advanced Bionics Corp., USA) implant in one patient, the Clarion II implant in one patient, the Clarion HiRes 90K implant in two patients, and the Nucleus Freedom (Cochlear Corp., Australia) Contour Advance in one patient. The control group was implanted with the MED-EL Combi 40? implant in 11 patients, the MED-EL Pulsar implant in 16 patients, the Clarion I implant in one patient, the Clarion II implant in two patients, the Clarion HiRes 90K implant in four patients, the Nucleus Freedom Contour Advance implant in two patients, and the Nucleus 24 Contour Advance implant in one patient. Surgical findings The senior author of this study and the same surgical team performed the surgical procedures. Perioperative findings were described as the presence of a cerebrospinal fluid (CSF) gusher, abnormality of the facial nerve, or other malformation around the temporal bone. Electrode insertion was performed via cochleostomy in 19 patients, by posterior labyrinthotomy in one patient, and by the round window in two patients. A perioperative CSF gusher occurred in 14 of 21 patients in the BLM group. Except for CC, all five IP-1 patients and nine IP-2 patients developed a gusher during the procedure. The cochleostomy was sealed with fat tissue and fibrin glue. The patient’s head was elevated postoperatively to manage the gusher. Except in two IP-1 patients, the gusher stopped with these interventions. For these two intractable cases, revision surgery was performed on the second postoperative day in one patient and in the third month in the other patient. Four patients had an anteriorly and laterally displaced facial nerve, which made the procedure risky. For this reason, cochleostomy could not be performed via a facial recess approach in two patients with CC and an abnormal facial nerve course. Therefore, the procedure was performed by the transcanal approach. In addition, in one patient with Klippel–Feil syndrome with neck anomaly and in another patient with a superiorly
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displaced cochlea, cochleostomy could not be performed via posterior tympanotomy. Their cochleostomies were performed via transcanal approach. In one patient who had IP-2, the fitting was unsatisfactory because of the vestibular displacement of the electrodes. This was diagnosed after the radiologic evaluation. This patient was again explored surgically and the electrode was correctly placed so that electrical stimulation was maintained adequately. On assessing commonly known late-type complications, we did not experience long-term complications in our BLM patients such as a late gusher or meningitis. Timing of the tests Speech and language development tests were performed for a median of 91 months (range 40–129 months) in the BLM group and for 96 months (range 42–139 months) in the control group. The difference was not statistically significant (p [ 0.05).
(range 4–7) in the control group and 5 (range 5–7) in the BLM group; the median SIR score was 4.5 (range 2–5) in the control group and 3 (range 2–5) in the BLM group) (p = 0.002 for CAP, p = 0.007 for SIR). The analysis of the speech perception test results, based on the specific type of malformation, showed that the both CAP and SIR scores were comparable between the IP-2, IP-1 and CC groups (p [ 0.05) (Table 3). Language development results The median receptive language development test score of the anomaly group was 22 (range 8–36) while median receptive language development test score of the control group was 27 (range 10–34) (p [ 0.05). Besides, the median expressive language development test score of the anomaly group was 22 (range 11–38) while median expressive language development test score of the control group was 28 (range 13–39) (p [ 0.05).
Speech perception and intelligibility results Discussion A comparison of the results of the CAP scores and SIR scores between the groups revealed that the scores in both test batteries were significantly higher in the control group than in the BLM group (the median CAP score was 7 Table 3 Patient details of the BLM group
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During the first years of the CI era, anomalous cochleae were a big problem for the neuro-otologists and there were several issues in performing the procedure. The first issue
Patient number
Type of BLM on implanted side
Type of CI
SIR score (category)
CAP score
1
IP-2
MED-EL Pulsar
2
5
2
IP-1
Clarion HiRes 90K
2
4
3 4
IP-2 IP-2
Clarion II MED-EL Pulsar
4 5
5 7
5
CC
MED-EL Pulsar
2
5
6
IP-2
MED-EL Pulsar
4
4
7
CC
MED-EL (Combi 40?)
3
4
8
IP-1
Clarion HiRes 90K
2
4
9
IP-2
Clarion I
2
3
10
CC
MED-EL Pulsar
3
6
11
IP-2
MED-EL Pulsar
5
7
12
CC
MED-EL (Combi 40?)
3
6
13
IP-2
MED-EL Pulsar
4
6
14
IP-2
MED-EL (Combi 40?)
5
7
15
IP-1
MED-EL Pulsar
3
5
16
IP-1
MED-EL Pulsar
3
5
17
IP-1
MED-EL Pulsar
4
6
18
CC
MED-EL (Combi 40?)
2
4
19 20
IP-2 IP-2
MED-EL (Combi 40?) Nucleus Freedom Contour Advance
4 5
6 7
21
IP-2
MED-EL (Combi 40?)
2
5
Eur Arch Otorhinolaryngol
was related to anatomical difficulties that make the procedure more challenging. The second issue concerned the sufficiency of the electrical stimulation of the cochlear neural structures provided by the cochlear implant. The third issue concerned the development of the auditory and linguistic skills of these groups of children after the operation. These issues are less problematic these days, although they still exist to varying degrees. For instance, our findings revealed that these groups of patients were more prone to surgical complications. The major challenge is the risk of having a CSF ‘‘gusher’’ occur intraoperatively. In particular, the IP-1 patients had a high incidence of experiencing a real ‘‘gusher’’ (i.e., not oozing) because of the large defect between the internal auditory canal and the malformed cochlea. However, other types of malformations are more prone to developing a gusher, compared to normal inner ears. In our series, a gusher occurred in all (100 %) of the 5 IP-1 patients, 9 (82 %) of 11 IP-2 patients, and 0 (0 %) of 5 CC patients. This indicates that 66.6 % (14 patients) of the 21 BLM patients had a gusher in our series. In other series, the approximate rate varies for a gusher occurring during the implantation of patients with a malformed inner ear. For example Hoffman et al. [12] found that 40 % of patients with BLM had a CSF gusher, regardless of the type of the malformation. Most reports reveal that the incidence of a gusher occurs in 40–50 % of patients with BLM [6]. Wootten et al. [13] reported the lowest percentage (1 %) of gushers in their patients. According to Papsin [14], the different percentages in the rate of gusher originated from the definition of the gusher. Papsin says the term ‘‘gusher’’ should be used only to describe the pulsatile outflow of the fluid and that minor egresses should not be described as a gusher. That is the source of the high incidences of gusher. In our opinion, our patients fulfill the gusher criteria and our rate is higher than most published rates. Another problem during the surgery of patients with BLM is the malpositioned facial nerve. As we noted in our series, four patients had an anteriorly and laterally displaced facial nerve, which made the procedure risky. For this reason, a cochleostomy could not be performed via facial recess approach in two patients with a CC and malpositioned facial nerve. They required a combined transcanal approach. In the literature, various reports indicate variability in the course of the facial nerve in patients with BLM [15–17]. Luntz et al. [18] and Khalessi et al. [19] reported patients with CC and a malpositioned facial nerve. Similar to Luntz and Khalessi, our two patients had a CC and we used a transcanal approach to perform a safe cochleostomy. An abnormal course of the facial nerve makes it more prone to surgical trauma, as Hoffman et al. [12] experienced with his patient. To secure the facial nerve during the procedure, some authors
recommend intraoperative monitoring of the nerve [6]. In our practice we do not use facial monitoring. Other important aspects of the implantation procedure for patients with BLM are (1) the cochlear implant provides sufficient electrical stimulation of the cochlear neural structures and (2) the development of the auditory and linguistic skills of these groups of children after the operation. In their study, Blamey et al. [20] state that at least 5,000 ganglion cells are required to achieve satisfactory speech perception after patients undergo CI. These statements and findings give hope because Schmidt [21] in a histological study found 7,677 cochlear neurons in a patient with Mondini dysplasia. From the histological level to the clinical end point (and paralleling the histological findings), various clinical studies demonstrate that patients with BLM who received CI can achieve audiological results comparable to those of patients who have a normal cochlear structure [17, 18]. In contrast to these histological and audiological findings, our results demonstrated that patients with BLM could not achieve results after CI that were comparable to those of patients who had a normal bony labyrinth with regard to speech perception (based on the CAP test) and speech intelligibility (based on the SIR tests). However, on analyzing the results based on the specific type of BLM, we showed that both the CAP and SIR scores were comparable between the specific type of malformations (IP-1, IP-2 and CC). In contrast to our findings about specific type of malformations, Mylanus et al. [22] conclude that severe malformations lead to poorer performances regarding speech perception tests. Actually the follow-up period of the patients in our study is longer than other studies in the literature. Different results regarding speech perception and intelligibility may attribute to different follow-up periods and also to the different number of patients (21 and 13 patients in our and Mylanus study, respectively). Our results concerning language development are comparable among the groups and indicate that patients who have BLM can achieve satisfactory results in the development of their linguistic skills that are comparable to the results of patients with normal bony labyrinths. Many authors have investigated the language development of patients after CI, although the authors focused on implantees with normal bony labyrinths [23, 24]. They showed that children could achieve satisfactory language development after CI. However, as Lee et al. [25] state, having an additional handicap such as mental retardation can have a negative impact on achieving satisfactory language development. We did not include any patient with mental retardation in our study group. In contrast to the speech development results, achieving comparable results in language development tests between the groups may indicate that it is not a substantial problem
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for implantees who have BLM to perform linguistic skills successfully after the CI procedure. Malformations such as IP or CC, based on their disordered cochlear structures, may diminish cochlear neuronal excitability or peripheral hearing; however, other skills such as language development could possibly survive because of their more complicated developmental process. We believe that proper assistance after implantation—especially audiological and linguistic rehabilitation administered by the audiology team and family support—could result in satisfactory linguistic skills.
8.
9.
10. 11. 12.
13.
Conclusion 14.
The data presented in this paper indicate that the CI procedure in children with BLM has some difficulties related to the surgical procedure and audiological outcomes. Peripheral hearing performances are significantly lower for patients with a BLM, although these patients and patients who have a normal bony labyrinth may improve their communication ability. Conflict of interest interest.
Authors declare that there is no competing
15.
16.
17.
18.
19.
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