An analysis of the inheritance pattern of an adult-onset hearing loss in Border Collie dogs

Although congenital (from birth) deafness has been widely recognised and reported in dogs, little has been done to characterise or study adult and geriatric onset deafness. The latter form of deafness is likely to represent a good model for human adult deafness (known as prebycusis). This study examines adult hearing loss in herding strains of Border Collies, a breed where owners have previously anecdotally reported adult onset deafness in their dogs. Border collies were examined using a standard established method to measure deafness in dogs (Brainstem Auditory Evoked Response (BAER)). Within a group of 216 dogs, five dogs over the age of 12 years had hearing loss, suggesting that a geriatric onset may be common in this cohort of dogs. A genetic component contributing to this form of deafness in dogs is suggested and discussed in the context of previous studies.

Although BAER hearing tests can be used to diagnose dogs with reduced hearing to an advanced stage and complete deafness, no diagnostic test is currently available for early identification of those Border Collies likely to become deaf. A recent study using some of the dogs reported here, but assuming an autosomal mode of inheritance and an earlier age of onset, and a GWAS approach, reported a region on CFA6 that appeared to be implicated [3]. An earlier smaller GWAS by some members of this group suggested a region on CFA18 [4].

Congenital Deafness has also been reported in Border Collies [5], assessed by BAER testing in 4–10 week old pups. Of 4143 pups tested, 2.4% had bilateral or unilateral deafness, which the authors state is a lower prevalence than found in other breeds. A large proportion of the deaf pups had either a blue iris color (58%) or a merle coat colour (26%), leading the authors to suggest the underlying genetic basis of their congenital deafness was related to a gene or genes that also affected pigmentation. Another study [6] of 2597 Border Collies, of which 2303 were puppies less than 9 weeks of age, also found that merle coat colour and blue eye color were contributing factors to congenital censorineural deafness. We did not examine or record eye color in the Border Collies in this study, but none of these dogs were merle coat colour.

Geriatric hearing loss, also known as presbycusis, is typically bilateral in humans [7]. The current study suggests that dogs over 12 may have deafness of this type (Figure  1) and therefore should be excluded in screens to find genes associated with adult-onset deafness. A study by ter Haar et al. [8] followed 10 mixed breed dogs with BAER testing at two year intervals, from 6 to 12 years of age. Although the mean dB threshold declined slightly between 8 and 10 years of age, the major decline in hearing was evident at all dB and all Hz at 12 years of age.

In 2000, in humans, approximately equal numbers of non-syndromic deafness were reported as inherited as autosomal dominant (31 DFNA) as autosomal recessive (28 DFNB) conditions, with few (6 DFN) X-linked conditions [9]. The Hereditary Hearing Loss Homepage [10] presents the genes associated with several forms of deafness in an expanded more current listing. Most forms of autosomal dominant deafness were reported as nonsyndromic and progressive [see Additional file 1]. Age of onset varied from childhood, often reported as postlingual, to about 50 years of age. Some forms began with hearing loss at high frequencies and others at low frequencies.

Most forms of progressive late onset adult deafness in humans have been reported to be inherited as dominant conditions [1]. One such form of sensorineural hearing loss (DFNA51) was reported to be caused by a tandem inverted duplication in the tight junction protein gene (TJP2) [11]. Another form is DFNA44, which is attributed to postlingual onset gradual disorganization of microtubule-based portions of the cytoskeleton in the pillar cells and stria vascularis, caused by a mutation in the CCDC50 gene [12]. However, the review by Domiguez and Dodson [1] reports that almost 30 genes have been reported to affect forms of autosomal dominant nonsyndromic hearing loss in humans, with 100 genes in all forms of deafness.

– Congenital deafness appears rare in Border Collies (1/216), although deafness from multiple possible causes was present in 11 of 216 dogs (5%) of various ages BAER tested at two herding field trials.

– At 12 years of age, 4 of 6 Border Collies BAER tested were deaf in one or both ears and this may suggest that geriatric hearing loss is common by this age in this breed.

– Adult onset bilateral deafness was not found in dogs under 3 years of age in the family studies and may begin as late as 7 years, based on BAER testing at the herding trials. Therfore many dogs will have been bred prior to the onset of this adult onset form of deafness.

– Adult onset deafness was perceived to have a gradual progression over years by the dog owners in both the family studies and field trial tested dogs. There is currently no diagnostic test to identify affected individuals until deafness becomes advanced, although higher dB levels of BAER testing than used in this study may have detected dogs at earlier ages.

– This adult onset deafness fits an autosomal dominant pattern of inheritance better than a recessive pattern.

“The data set supporting the results of this article is included within the article (and Additional file 1)”.

In accordance with Canadian Animal Care Guidelines, signed written consent was obtained from all dog owners prior to BAER testing and DNA sampling. This consent form includes permission for publication of these data.