Research paperInteraural comparison of spiral ganglion cell counts in profound deafness☆
Highlights
► SGCs were counted in both temporal bones from symmetrically deafened humans. ► The variance in total SGC count of one ear accounts for 98% of the other’s variance. ► Realistic sample sizes (10) reliably detect unilateral treatment effects (1000 SGCs).
Introduction
Spiral ganglion cells (SGCs), the first-order neurons of the auditory system, have been the subject of many studies. For example, the number of these cells in normal-hearing ears (Guild, 1932) and in hearing-impaired ears with different etiologies (Nadol et al., 1989) has been reported. One question that has not been directly studied is whether the difference in the number of SGCs between ears of an individual is small when the hearing sensitivity is similar. This is of interest because a small difference would imply that one ear could be used as a control ear in temporal bone studies evaluating the impact on SGC survival of a treatment, insult or some other factor experienced only by the other ear.
When matched for hearing sensitivity, the relatively large, across-subject variation in the SGCs counted leads one to question whether a similar variation holds across ears in the same subject. For temporal bones from subjects with normal-hearing sensitivity while living, Guild (1932) documented a range of 23,193 to 39,114 total SGCs (N = 10) and Otte et al. (1978) reported approximately 20,000 to 37,000 SGCs (estimated from their Fig. 3; N = 8). The range can be even larger in the case of subjects who suffered significant hearing impairment. In 16 temporal bones from subjects with documented pure tone threshold average greater than 70 dB HL during life, Hinojosa and Marion, 1983 reported counts of total SGCs ranging from 0 to 25,873 SGCs (N = 16). If the relatively large across-subject variability in SGC counts seen in both normal and hearing-impaired ears is also exhibited between ears in the same subject, the use of one ear in each subject as a control for the other would provide relatively weak statistical power.
In spite of this potential problem, it is not unusual for investigators to use one ear as a control for the other in temporal bone studies. For instance, Khan et al. (2005) studied the effect of cochlear implantation on SGC survival by assuming both ears of an implantee had the same number of SGCs before implantation and compared the SGC count of the implanted ear with that of the contralateral ear. Fayad and Linthicum, 2006 made the same assumption and evaluated the effect of multi-channel cochlear implants on different elements of temporal bone histopathology (including SGC count) by comparing the implanted with the non-implanted ear. Except for Nadol et al. (1989) who reported a correlation of 0.87 between the SGC counts of the right and left ears of 27 subjects (not selected for symmetric hearing sensitivity), there is little basis for assuming the SGC count for one ear can serve as an effective control for the opposite ear.
The present study evaluates the degree to which the SGC counts in the left and right temporal bones of 21 subjects who were profoundly hearing impaired during life are similar. We also demonstrate how the results can be used in statistical power calculations to help guide the design of experiments using one ear of each temporal bone pair as a control for the other.
Section snippets
Methods and materials
The 42 temporal bones from 21 subjects (Table 1) selected for study included a subset of bones from the 93 temporal bones of 66 profoundly hearing impaired individuals studied by Nadol et al. (1989) meeting the following criteria: (1) the right and left temporal bones of each subject are available, (2) same etiology for hearing loss in both ears in each subject and (3) bilaterally symmetric profound hearing impairment documented by a statement in the medical history or by audiometric test
Results
Table 1 shows that the 21 cases were impaired by a variety of etiologies including congenital malformations such as Mondini and CHARGE associated cochlear malformation, and acquired diseases such as viral labyrinthitis. The subjects included 11 males and 10 females ranging in age from 0.6 to 92 years at the time of death. There was a wide range of the duration of deafness that varied between a few months in cases 13 and 3 to more than 80 years in cases 7 and 10.
While the medical history of each
Discussion
The results presented for the 21 subjects with bilaterally symmetric profound hearing loss indicate that the within-subject between-ear differences in SGC counts were relatively small. An example set of power analysis calculations lead to the conclusion that realistic sample sizes (e.g., 10–20) are sufficient to reliably detect treatment effects on the order of 1,000 SGCs in temporal bone populations similar the one studied here.
One question that arises when these results are to be applied to a
Conclusion
Histological examination of 21 pairs of temporal bones from bilateral-symmetric profoundly-impaired ears found relatively small within-subject between-ear differences in counts of spiral ganglion cells. Results also suggest that realistic sample sizes (e.g., 10 to 20 subjects) are sufficient to reliably detect unilateral treatment effects on the order of 1,000 SGCs in temporal bone populations similar to the one studied when one ear is used as a matched control for the treated ear.
Acknowledgment
This work was supported by grant R01-DC00152 from the National Institute of Deafness and Other Communication Disorders.
References (12)
Quantification of human spiral ganglion cells by serial section reconstruction and segmental density estimates
Am. J. Otolaryngol.
(1988)- et al.
Temporal bone anomaly proposed as major criteria for diagnosis of CHARGE syndrome
Am. J. Med. Genet.
(2001) - et al.
Spectrum of hearing disorders and their management in children with CHARGE syndrome
Otol. Neurotol.
(2010) - et al.
Multichannel cochlear implants: relation of histopathology to performance
Laryngoscope
(2006) Correlations of histologic observations and the acuity of hearing
Acta Oto-larygol
(1932)- et al.
Histopathology of profound sensorineural deafness
Ann. N. Y Acad. Sci.
(1983)
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This work was supported by grant R01-DC00152 from the National Institute of Deafness and Other Communication Disorders.