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. Author manuscript; available in PMC: 2025 Mar 1.
Published in final edited form as: Otol Neurotol. 2024 Jan 17;45(3):245–255. doi: 10.1097/MAO.0000000000004102

Intracochlear trauma and local ossification patterns differ between straight and pre-curved cochlear implant electrodes

Alexander Geerardyn a,b,c,d, MengYu Zhu b, Nicolas Verhaert c,d, Alicia M Quesnel a,b
PMCID: PMC10922381  NIHMSID: NIHMS1949515  PMID: 38270168

Abstract

Hypothesis

Trauma to the osseous spiral lamina (OSL) or spiral ligament (SL) during cochlear implant (CI) insertion segregates with electrode type and induces localized intracochlear ossification and fibrosis.

Background

The goal of atraumatic CI insertion is to preserve intracochlear structures, limit reactive intracochlear tissue formation, and preserve residual hearing. Previous qualitative studies hypothesized a localized effect of trauma on intracochlear tissue formation; however, quantitative studies failed to confirm this.

Methods

Insertional trauma beyond the immediate insertion site was histologically assessed in 21 human temporal bones with a CI. 3D reconstructions were generated and virtually re-sectioned perpendicular to the cochlear spiral at high resolution. The cochlear volume occupied by ossification or fibrosis was determined at the mid-point of the trauma and compared to regions proximal and distal to this point.

Results

Seven cases, all implanted with pre-curved electrodes, showed an OSL fracture beyond the immediate insertion site. Significantly more intracochlear ossification was observed at the mid-point of the OSL fracture, compared to the −26° to −18° proximal and 28° to 56° distal to the center. No such pattern was observed for fibrosis. In the twelve cases with a perforation of the SL (9 straight and 3 pre-curved electrodes), no localized pattern of ossification or fibrosis was observed around these perforations.

Conclusion

OSL fractures were observed exclusively with pre-curved electrodes in this study and may serve as a nidus for localized intracochlear ossification. Perforation of the SL, in contrast, predominantly occurred with straight electrodes and was not associated with localized ossification.

Introduction

A cochlear implant (CI) is a surgically implantable device that can help people with severe to profound hearing loss to regain their ability to perceive speech1. In recent decades, there has been a growing interest in mitigating the acute insertion trauma that was previously regarded as inevitable. For, example, pre-curved (peri-modiolar) electrodes have been designed to limit the lateral wall trauma typically occurring with straight (lateral wall) electrodes and position the CI electrodes closer to the spiral ganglion neuron cell bodies.

Atraumatic CI insertion is considered crucial for the preservation of residual acoustic hearing. When preservation of any residual hearing is used as a surrogate for atraumaticity, atraumatic insertion has been shown to be beneficial for speech perception with the electrical stimulation by the CI alone2. In addition, atraumatic CI insertion may help to preserve the possibility of future regenerative therapies.

CI insertion trauma has two components: (1) the acute damage to intracochlear structures, such as the spiral ligament (SL), osseous spiral lamina (OSL), or basilar membrane, and (2) the subsequent healing response mediated by inflammatory processes3–6. Over time, these inflammatory processes result in a foreign body effect consisting of intracochlear fibrosis and ossification4,7. Intracochlear ossification has been linked to poorer speech perception with the CI8 and could potentially cause a loss of residual hearing9–12. Moreover, fibrosis and ossification around the electrode cause increased electrode impedances and overall power consumption of the device13–15.

Results from both animal and human temporal bone (HTB) studies indicate that a higher degree of acute insertional trauma could result in increased intracochlear fibrosis and ossification5,7,8,16–19. Multiple quantitative studies have shown a larger degree of intracochlear tissue formation at the cochlear base following cochleostomy (CO) or extended round window (RW) insertions compared to the less traumatic RW insertions20–22. While some qualitative studies also describe a localized effect of acute trauma beyond the immediate insertion site on intracochlear tissue formation7,16,17,23, previous quantitative studies in human post-mortem temporal bones failed to confirm such an effect.8,18

The aim of the present study is to quantitatively assess the relationship between two types of acute insertional trauma beyond the immediate insertion site – i.e., SL perforation and OSL fracture - and chronic intracochlear fibrosis and ossification. 3D reconstructions generated from histological sections of human post-mortem temporal bones allow us to accurately calculate the volumes of intracochlear fibrosis and bone. Moreover, by applying the recently developed method of automated virtual re-sectioning at high resolution along the cochlear duct9, we are able to analyze the localized effect of intracochlear trauma. We hypothesize that the trauma pattern segregates with electrode type (pre-curved vs straight) and that cases with signs of acute insertional trauma to the SL or OSL will show higher levels of intracochlear tissue formation compared to the cases without trauma beyond the immediate insertion site. Moreover, we expect a localized increase of fibrosis and ossification centered around the trauma.

Methods

Specimens

The present study is conducted on the histological preparations of post-mortem HTB specimens of donors who received a CI during life. All specimens were processed for light microscopic study in a standardized multi-step process including formalin fixation, decalcification, dehydration in serially diluted alcohols, and embedment in celloidin.24 Subsequently, the embedded specimen is horizontally sectioned at 20 μm thickness. Finally, every tenth section is stained with hematoxylin and eosin, mounted, and scanned with an Aperio AT2 scanner (Leica Biosystems, Germany). The CI electrode array was removed prior to embedment to allow for sectioning without damaging the knife.

The HTB specimens were selected from the Massachusetts Eye and Ear (MEE) Otopathology Laboratory collection. Starting from all 71 CI specimens embedded in celloidin, only specimens with a CI electrode initially inserted into the scala tympani (ST) were included in this study. Cases with congenital anomalies, a history of meningitis, a history of a temporal bone fracture including the otic capsule, or implantation with the highly traumatic Symbion Ineraid electrode or electrode positioner were excluded. Ultimately 21 cases were included in this study. Some of these cases were included in previous histopathological studies8,9,18,22, though the current analysis of the local relationship between insertional trauma and intracochlear tissue formation by application of the virtual resection method has not been performed before.

Specimens were assigned to the straight or pre-curved electrode group based on the design of the electrode array, not the ultimate position in the cochlea.

Histological assessment

For every specimen, each stained section was evaluated for signs of acute insertional trauma at the SL (0: intact, 1: perforation) or OSL (0: intact, 1: Fracture). We chose not to focus on basilar membrane elevation/rupture because this tended to be diffusely present when it occurred. Moreover, this delicate structure can sometimes be artifactually disrupted during removal of the CI array. As we focused on the relationship between intracochlear trauma beyond the immediate insertion area and fibrous and bony tissue formation, we only reported the SL perforation or OSL fractures occurring beyond 45 ° of insertion depth.

The insertion location (i.e., RW, ERW, or CO) of the CI electrode array was assessed on histology. The CO insertions were histologically distinguished from the ERW insertions based on the presence of a bony bridge between the electrode insertion path and the RW membrane.

3D reconstructions and virtual re-sectioning

A 3D reconstruction was generated for every specimen based on the digitized histological sections and subsequently virtually re-sectioned perpendicular to the cochlear spiral (Amira 2019.1; Thermo Scientific). This methodology has recently been developed for a study on the potential impact of intracochlear tissue on the inner ear mechanics.9 In brief, first the electrode trajectory, perilymph, fibrosis, and ossification were manually segmented on every digitized section and used to generate a 3D reconstruction. Subsequently, the 3D reconstructions were virtually re-sectioned perpendicular to the cochlear spiral at fixed intervals of 2 degrees from the mid-point of the trauma (See Figure 1). The angular locations along the cochlear spiral were calculated based on the coordinate system described by Verbist et al.25 Finally, for each of these sections, the absolute volumes of intracochlear fibrosis, ossification, or normal perilymph were calculated by multiplying the number of voxels in that specific section with the voxel volume.

Figure 1: Virtual re-sectioning of 3D reconstruction at angular locations around trauma.

Figure 1:

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The upper left panel shows the 3D reconstruction of case 18 with an isolated osseous spiral lamina fracture at about 123° insertion depth. The locations of virtual re-sectioning are indicated by the red boxes. For visual purposes only locations −30°, 0°, and 30° relative to the middle of the osseous spiral lamina fracture are displayed. The three other panels show the result of the virtual re-sectioning with different colors indicating different intracochlear tissues. Yellow indicates the location of the electrode array; Blue indicates normal perilymph; Grey indicates fibrosis; White indicates ossification. Scale bars in the upper left panel measure 1mm.

Statistics

Statistical tests were performed with MATLAB R2021b. Normality was assessed with a Kolmogorov-Smirnov test with Lilliefors Modification. The significance level was set at 0.05. All tests are two-sided unless explicitly stated.

Results

Implantation characteristics

The present study included 11 and 10 cases implanted with straight or pre-curved electrode designs, respectively. Specific implant and electrode types are displayed in Table 1. The insertion location was histologically categorized as ERW, CO, or RW in 17, 3, and 1 cases respectively. The mean duration of implantation was 89 months (SD 60 months). The angular insertion depth of the CI electrode ranged from 114° to 576 ° (Mean 379°; SD 124°).

Table 1: Case demographics, electrode type and insertional trauma.

Asterisks indicate bilateral implants from the same individuals. R: Right; L: Left; ERW: Extended Round Window; CO: Cochleostomy; RW: Round Window; SL Perf: Spiral ligament perforation; OSLFx: Osseous Spiral Lamina Fracture.

Case Side Electrode Group Implant/Electrode Type Year of implantation Insertion Location Duration of implantation (months) Angular Insertion Depth (°) SL perf OSLFx
1 R Straight Nucleus 22 1988 ERW 81 147 N N
2 R Straight Nucleus 22 1988 ERW 139 322 N N
3 L Pre-Curved Nucleus 24 Contour CI24R(CS) 2003 ERW 83 524 N N
4 L Pre-Curved Nucleus 24 Contour CI24R(CS) 2000 ERW 127 393 N N
5 R Pre-Curved Nucleus 24 Contour CI24R(CS) 2007 CO 82 483 N N
6 L Straight Nucleus 22 1990 ERW 133 261 Y N
7 R Straight Nucleus 22 2002 ERW 28 347 Y N
8 R Straight Nucleus 24 2000 ERW 79 300 Y N
9 L Straight Nucleus 1989 ERW 210 321 Y N
10* R Straight Nucleus 22 1990 ERW 244 257 Y N
11 L Straight Clarion CII 2003 ERW 101 326 Y N
12 L Straight Nucleus Hybrid 6 S8 2006 CO 75 114 Y N
13 R Straight AB HiRes 90K 1J 2012 ERW 12 433 Y N
14 R Straight MED-EL Synchrony Medium 2015 RW 49 576 Y N
15 L Pre-Curved AB HiRes 90K Helix 2005 CO 94 553 Y Y
16** L Pre-Curved AB HiRes 90K Helix 2012 ERW 19 494 Y Y
17 R Pre-Curved Nucleus CI24RE(CA) 2010 ERW 79 502 Y Y
18* L Pre-Curved Nucleus 24 Contour CI24R(CS) 2006 ERW 47 428 N Y
19 R Pre-Curved AB HiRes 90K Helix 2009 ERW 33 388 N Y
20** R Pre-Curved AB HiRes 90K Helix 2012 ERW 19 379 N Y
21 L Pre-Curved AB HiRes 90K Helix 2008 ERW 132 420 N Y
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Trauma

Five cases (24%) showed no trauma to the SL or OSL beyond the immediate insertion location. An isolated SL perforation (without OSL fracture) was observed in nine cases (43%), and an isolated OSL fracture (without SL perforation) was observed in four cases (19%). Finally, three cases (14%) showed both a SL perforation and an OSL fracture.

Overall, electrode translocation from ST to scala vestibuli/media occurred in 11/21 cases. Of the seven cases with an OSL fracture, four (57%) were translocated. Of the 12 cases with a SL perforation, translocation occurred in 10 (83%).

Examples of histological sections with intracochlear trauma are displayed in Figure 2.

Figure 2: Histological Sections showing intracochlear trauma.

Figure 2:

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A-B: Case 10 with isolated spiral ligament perforation (blue arrow). Panel B is the magnification of the red box area in panel A. C-D: Case 17 with combined osseous spiral ligament perforation (blue arrow) and osseous spiral lamina fracture (red arrow). Panel D is the magnification of the red box area in panel C *: Electrode array; +: intracochlear fibrosis; ++: intracochlear bone formation; T: Scala tympani; V: Scala vestibuli; M: Scala media.

Figure 3 shows the angular insertion depth and locations of trauma along the cochlear spiral for each of the individual cases included (See supplementary table for the exact angles). SL perforations had their starting point in the basal turn between 90° to 161°. The OSL fractures covered a wider range of starting points from 63° to 230°. The angular length of SL perforations (N=12; Mean: 174°; SD 147°) was significantly longer (two sample t-test: p = 0.04) than the angular length of the OSL fractures (N=7; Mean: 45°; SD 31°).

Figure 3: Angular insertion depth and locations of trauma.

Figure 3:

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Each line resembles the uncoiled cochlear spiral of one individual case. The electrode insertion depth, spiral ligament perforation or osseous spiral lamina fracture locations are indicated in yellow, blue, and red, respectively. See Supplementary table for angles of start, middle, and end of the trauma. SL: Spiral Ligament; OSL: Osseous spiral lamina.

In the present sample, of the 12 SL perforations observed, 9 (75%) occurred in cases implanted with a straight electrode design. OSL fracture was observed exclusively (100%) in cases implanted with a pre-curved electrode design. None of the cases with a straight electrode design showed a fracture of the OSL beyond the immediate insertion site. (Figure 4).

Figure 4: Trauma pattern in cases with a straight vs pre-curved cochlear implant electrode beyond the immediate insertion site.

Figure 4:

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For each angular location along the cochlear spiral (black line) the proportion of cases showing a spiral ligament perforation or osseous spiral lamina fracture are indicated in blue and red, respectively. Darker colors indicate a larger proportion of cases showing trauma at that specific angular location. SL Perf: Spiral ligament perforation; OSLFx: Osseous Spiral Lamina Fracture. See Supplementary table for angles of start, middle, and end of the trauma. Trauma at the insertion site < 45° is not shown on this figure.

Total tissue formation

The average proportion of the cochlear volume occupied by new tissue formation was 32% (SD 14%), composed of 25% (SD 12%) fibrosis and 7% (SD 6%) ossification. We observed a significantly lower proportion of total intracochlear tissue formation in cases with no trauma beyond the immediate insertion site (n = 5; mean 18%) compared to those with a SL perforation (n = 9; mean 33%; two sample t-test, p = 0.02) or OSL fracture (n = 4; mean 42% two sample t-test, p = 0.01). As displayed in Figure 5, a similar trend was observed for the cases with both a SL perforation and OSL fracture, though because of the limited power of the test (1- β = 0.45) given the small sample sizes, no significant difference was observed (n= 3, mean 39%; two sample t-test, p = 0.07).

Figure 5: Proportion of Cochlear Volume Occupied by Fibrosis or Bone in cases with different trauma patterns.

Figure 5:

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SLPerf: Spiral ligament perforation; OSLFx: Osseous Spiral Lamina Fracture.

We observed no significant difference in total intracochlear tissue formation between cases implanted with a pre-curved (N = 12; Mean 35%) or straight electrode design (N = 9; mean 29%; two-sample t-test, p = 0.31).

Furthermore, no significant correlation was observed between the angular length of the SL perforation or OSL fracture and the proportion of intracochlear tissue formation (Pearson Correlation, p > 0.05)

Localized tissue formation

Figure 6 shows the localized intracochlear tissue formation around the midpoint of the OSL fracture (Panel A & B) and SL perforation (Panel C & D).

Figure 6: Localized intracochlear tissue formation around the midpoint of insertional trauma.

Figure 6:

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Each panel shows on the y-axis the proportion of the cochlea filled with bone (A & C) or fibrosis (B & D). The proportion of intracochlear tissue is centered around the midpoint (0°) of the trauma for each case. Negative angles indicate a more basal location, positive angles indicate a more apical location. The upper panels show the cases with an OSL fracture, the lower panels the cases with a SL perforation. Each case is plotted individually in a different color. The red line indicates the mean of all specimens at that point. The shaded areas show the locations where the intracochlear tissue formation is more than 5% and significantly lower than at the midpoint (0°) (one-sided t-test, p < 0.05).

We observed a localized effect of the OSL fracture on intracochlear ossification with significantly lower (paired t-test, one-sided) intracochlear bone formation in the region from −26° to −18° proximal, and 28° to 56° distal to the OSL fracture compared to the degree of ossification at the midpoint. When looking at each of the 7 cases with an OSL fracture individually, we observed a clear pattern of ossification centered around the middle of the OSL fracture in 4/7 cases (case 16, 17, 18, 20). For cases 15 and 19 little to no ossification was observed around the OSL fracture. Finally, for case 21 there was a large proportion of ossification around the midpoint of the OSL fracture, but the localized pattern was not as clearly visible because of the large proportion of intracochlear ossification proximal to the OSL fracture – close to the insertion area.

Regarding fibrosis around the OSL fracture, we observed a similar trend towards a localized effect on total intracochlear tissue formation, however, only the intracochlear tissue formation at the distal - not the proximal – locations was significantly lower than at the midpoint (paired t-test, one-sided: p>0.05).

Around the middle of the SL perforations, we did not observe a localized effect for ossification or fibrosis. While some individual cases showed ossification or fibrosis around the middle of the trauma, on average significantly lower intracochlear fibrosis was observed only at the distal locations > 70° (not proximal to the SL perforation)

There was no significant correlation between the duration of implantation and the degree of ossification around the local midpoint of trauma (Pearson correlation, p>0.05) despite the significant positive correlation between the duration of implantation and the total cochlear volume of ossification (Pearson Correlation; Rho 0.49; P=0.02).

Discussion

Acute insertional trauma

In this study, we analyzed acute insertional trauma specifically at the OSL and SL. This is in contrast with the widely used trauma score developed by Eshraghi and colleagues.26 The Eshraghi score is relevant to study the trauma mechanisms occurring at the lateral or medial wall. However, by combining trauma to multiple structures in one level, it does not allow to assess the localized effect of insertional trauma to one isolated intracochlear structure.

In 76% of cases included in this study, insertional trauma to the SL or OSL was observed beyond the immediate insertion site. Figure 4 shows the distinct trauma patterns in straight versus pre-curved electrodes beyond the immediate insertion site. It is noted that the cases with straight electrodes exclusively showed trauma to the SL at the lateral wall of the cochlea, whereas cases with pre-curved electrodes predominantly showed trauma at the OSL.

It is known that straight electrodes mainly impact the lateral wall.7,27,28 Given the cochlear anatomy and the electrode design, contact with the lateral wall of the ST is inevitable. With high insertion forces, this may cause perforation of the SL at the lateral wall.29 In the present study, SL perforation was present in 82% of cases with a starting point at an angular insertion depth of 90°−161°. This angular location is in line with previous studies29–31 and can be attributed to the changes in ST dimensions along the cochlear duct.32,33

Limiting lateral wall trauma was one of the main goals in the design of pre-curved electrodes.34 In the current sample, SL perforation was indeed less frequent in cases implanted with pre-curved electrodes. It is, however, important to note that the present study only includes pre-curved electrode designs without positioners. The old positioners are known to cause extensive lateral wall trauma because of their large volume.35,36

Although the pre-curved electrode designs largely succeeded in limiting trauma to the lateral wall of the ST, the OSL appears to be at increased risk of insertional trauma.26 In the present sample, OSL fracture was observed in 70% of cases implanted with a pre-curved electrode. In contrast, none of the cases with a straight electrode design showed an OSL fracture beyond the immediate insertion location. Previous studies, however, did show that OSL fractures can also occur with straight electrode designs, especially when insertion is continued after buckling of the electrode.27,31,37

SL perforations occurred over a significantly longer angular distance than OSL fractures. This may be attributed to the soft tissue vs bony nature of both structures. Moreover, we hypothesize that electrode design may play a role. Most SL perforations (75%) in the current sample occurred with straight electrode designs and since straight electrodes do not have a mechanism to curve the electrode array, it does not pass back into the scala (tympani or vestibuli) until the electrode itself bends against the lateral wall. In contrast, all OSL fractures occurred with pre-curved electrode designs, and we hypothesize that their curvature and stiffness might cause the electrode to translocate or relocate over a shorter angular distance. The current methodology, however, does not allow to test this hypothesis.

Furthermore, it is important to note that the absolute rates of trauma observed in the present sample may not be representative of CI insertions today. First, many of the implantations included date back from a time before the widespread awareness of the benefits of atraumatic insertion.2 Second, not only the surgical techniques but also the electrode designs have evolved over time resulting in lower insertional trauma rates, at least in acute insertion studies.28,38–41 Third and finally, the distribution of the different electrode insertion locations in this study is skewed towards ERW insertions, while it is known that the insertion location of the electrode may impact the electrode trajectory and trauma pattern.37,40,42 Future insertions may be even less traumatic with robotic insertion and the integration of insertion tools that can help direct the electrode array in the cochlea away from delicate structures in real time.43,44

Intracochlear tissue formation in cases with or without insertional trauma

Our observation that the proportion of intracochlear tissue formation is higher in cases with acute insertional trauma is in line with previous HTB studies7,8,16–18. While some of these studies described this association based on a qualitative assessment7,16,17, others actually calculated the volumes of intracochlear fibrosis and ossification to analyze this relationship.8,18 In the current study, we present further evidence on the association between acute insertional trauma and total volumes of intracochlear tissue formation. Moreover, for the first time, we present data on the localized impact of insertion trauma beyond the immediate insertion site by applying the recently developed method of automated virtual re-sectioning at high resolution along the cochlear duct.9

We observed an association between the presence of an OSL fracture and total volume of intracochlear fibrosis and ossification (Figure 5). This finding is in line with the findings from an experimental animal study in guinea pigs.19 In a similar human post-mortem study, however, Kamakura and Nadol failed to observe such an association for OSL alone.8 These conflicting results may be attributed to the way this association was investigated in the two studies. In the present study, on the one hand, we compared groups with or without OSL trauma and found a significant difference in intracochlear tissue formation. Kamakura and Nadol, on the other hand, calculated the correlation between the extent of trauma to the OSL along the cochlear duct and the volumes of intracochlear tissue formation.8

More interestingly, the localized tissue formation data unique to the present study show significantly more ossification around the middle of the OSL fracture compared to about 30 degrees proximal and distal to the trauma. (Figure 6A). This indicates that an OSL fracture could have a local ossification-inducing effect. On an individual case level, we noted a considerable amount of intracochlear ossification around the middle of the OSL fracture in 5/7 cases. In four of these cases with considerable ossification, we observe a clear localized pattern around the OSL trauma. In case 21, however, this localized pattern is less explicit because of the high degree of tissue formation proximal to the OSL. In this specific case, the localized effect may be hidden in the substantial volume of ossification extending from the insertion location at the base, typically seen with ERW or CO insertions.9,20,21 In two cases, case 15 & 19, little ossification is observed. It is unclear which factors have prevented the ossification effect observed in the other cases.

When looking at fibrosis instead of ossification, we observe, on average, a slight increase in fibrosis around the center of OSL (Figure 6B). This trend, however, is not statistically significant and except for case 16, none of the individual cases showed such a localized pattern.

While the OSL fractures occur medially in the ST, the presence of a SL perforation indicates trauma to the lateral wall. In the present study, we confirm the findings from Li and colleagues that lateral wall trauma is associated with an increased volume of intracochlear fibrosis and ossification.18 While in some qualitative assessments, a localized relationship between lateral wall trauma and intracochlear tissue formation was observed7,17, Li and colleagues18, failed to observe such localized effect in their quantitative assessment. Our 3D quantitative volumetric results from localized tissue formation around the center of the SL perforation are in line with these prior quantitative findings, showing no localized effect of SL perforation on fibrosis or ossification (Figure 6C & 6D).

The significantly lower degrees of fibrosis distal to the OSL fracture or SL perforation (Figure 6B & 6D), without significantly lower degrees proximal to the trauma, are not sufficient to infer a localized effect, as a gradient from base to apex is a typical finding4,7,17 and is attributed to the absence of the electrode array distally.

It was beyond the scope of the current study to compare speech perception scores with different electrode types. Previous clinical outcome studies comparing straight vs pre-curved electrodes have shown conflicting results regarding which electrode type leads to better speech perception outcomes.45–47 We hypothesize that the distinct trauma pattern and localized ossification between electrode types may account for some of the variability in speech perception outcomes. In the current study, we found that pre-curved electrodes were associated with OSL fractures and localized ossification, whereas straight electrodes were not. Interestingly, a previous study showed that the cochlear volume of ossification was negatively correlated with speech perception with the CI8. We hypothesize that in cases with pre-curved electrodes, part of the beneficial effects on speech perception of the more peri-modiolar electrode location48 may be neutralized by the higher rate of OSL fractures and associated localized ossification.

Contribution of insertional trauma to intracochlear fibrosis and ossification

The present study further supports the hypothesis that acute insertional trauma contributes to the chronic intracochlear fibrosis and ossification after implantation.3–5,19 Previous animal studies indicated that acute insertional trauma augments the acute inflammatory response, resulting in a more extensive chronic foreign body response to the CI electrode with associated intracochlear fibrosis and ossification.5,6,49 Damage to the endosteum and other soft tissue structures in the cochlea associated with perforation of the SL at the lateral wall may induce increased acute inflammation. Moreover, trauma to the abundant blood vessels in the SL and stria vascularis could result in intracochlear bleeding, which has recently been shown to be associated with increased acute inflammation and chronic intracochlear fibrosis.27,49 Our results further indicate that these processes do not seem to occur locally around the SL perforation but rather have effects throughout the entire cochlea resulting from the spread of the inflammatory cells and mediators in the cochlear fluids.18

Yet, around the OSL fractures, we did observe localized ossification. This may indicate that an OSL fracture during CI electrode insertion disturbs the unique balance of bone remodeling in the inner ear.50–52 By disturbing this balance, the existing inhibition of bone remodeling that, for example, prevents bony union after a temporal bone fracture53, can be lifted, allowing for ossified healing around the OSL fracture. Based on the present study we cannot identify exactly how the OSL fracture during CI electrode insertion affects the cellular processes and signaling cascades involved in normal fracture healing. Potential factors may include the increased levels of inflammatory mediators after CI insertion5,6,49 or lower levels of osteoprotegerin, a potent inhibitor of bone remodeling.50–52 Our observation that in two of the seven cases with an OSL fracture, no ossification around the middle of the OSL fracture was observed, indicates that multiple factors may need to be present in order to allow for ossification around the OSL fracture to occur.

Limitations

Despite its multiple advantages, human post-mortem histology has some limitations. First, because of the inherent delay between the time of implantation and time of death, we are limited to studying the impact of older electrodes and older surgical techniques. Although the induced acute trauma may be lower nowadays, the present sample still allows to investigate the effect of acute insertional trauma on the chronic intracochlear tissue formation and mechanisms that are distinct between straight and pre-curved electrodes. Second, inherent to the methodology of HTBs, fibrosis and ossification can only be evaluated at a single time point, thereby not allowing for definite statements on how acute insertional trauma translates into chronic fibrosis or ossification. Third, the overall number of HTB specimens with a CI is limited resulting in relatively small sample sizes when comparing different subgroups.

Conclusion

In summary, the present study supports the hypothesis that acute CI insertional trauma contributes to localized chronic intracochlear ossification at the site of injury, and that the patterns of acute injury and chronic intracochlear tissue deposition segregate based on pre-curved vs straight electrode designs. In this sample of 21 human post-mortem temporal bones with a CI, the cases with a fracture of the OSL or perforation of the SL showed significantly higher degrees of total intracochlear tissue formation at the time of death than those without trauma. Moreover, for the first time in HTBs, a localized ossifying effect was shown around the OSL fractures with significantly more ossification at the middle of the fracture compared to about 30 degrees more to the base or to the apex. No such localized effect was observed around SL perforations. This indicates that a fracture of the OSL during CI insertion may serve as a nidus for localized intracochlear ossification while perforation of the SL seems to have a more generalized effect.

Supplementary Material

Supplemental Digital Content

Acknowledgments

The authors express their gratitude to Joseph B. Nadol Jr. MD for his contributions in beginning and building the post-cochlear implant temporal bone collection at Mass. Eye and Ear. We also wish to thank Anbuselvan Dharmarajan MD, Diane Jones, and Barbara Burgess for their assistance in processing the histological specimens, as well as Haobing Wang and Peizhe Wu MD for their support with the software. Additionally, the authors would like to acknowledge the donors who generously pledged their temporal bones through the NIDCD National Temporal Bone Resource Registry which were used in this study.

Conflicts of Interest and Sources of Funding

This work was financially supported by Research Foundation Flanders (FWO: 1SD3322N(AG), V414121N(AG), 1804816N(NV), G088619N(NV)) and NIH/NIDCD (U24DC013983(AMQ), U24DC020849(AMQ), R01DC021606(AMQ)).

Alicia M. Quesnel, MD: Grace Medical - sponsored research agreement; Frequency Therapeutics - sponsored research agreement, consulting; Alcon – consulting.

The other co-authors have no conflict of interest to declare.

List of Abbreviations

CI

Cochlear Implant

CO

Cochleostomy

ERW

Extended Round Window

HTB

Human Temporal Bone

OSL

Osseous Spiral Lamina

SL

Spiral ligament

ST

Scala tympani

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