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Hearing loss and noise effects in hearing are commonly known in humans. But how does hearing loss develops in animals in their auditory system, what are the pathophysiological mechanisms, and what is the most prevalent type of hearing loss in animals?

The type of hearing loss is subdivided into three categories: Sensorineural, transmission, or mixed. In animals, hearing loss can arise in several ways, one of them is related to prolonged exposure to loud sounds, both infrasound or ultra sounds. To determine the etiology of hearing loss in animals, tests are performed with or without anesthesia. In this way, it is still possible to study which are the most advantageous forms of treatment that can benefit not only animals but also humans. Like humans, hearing in animals can deteriorate with age and each species is affected differently by exposure to noise.

Animals can also experience annoying buzzing. To prove the occurrence of this symptom, various means and techniques are used. No cure has yet been discovered, it is important to continue to investigate the origin of tinnitus and its different types. Another important aspect to highlight is to know the causes that lead to hearing loss in animals.

The purpose of this review is to study hearing loss in animals, determine what kind of hearing loss is more prevalent, the possible symptoms and the tests that are used to assess hearing in animals. Translational knowledge (from animals to humans) is relevant.

Hearing loss and tinnitus in animals

Hearing loss can be observed in all animal species [1]. The type of loss can be subdivided in sensorineural (who arises from an injury to the inner ear, and can extend through the auditory nerve, where hair cell loss occurs), transmission (affecting the outer and/or middle ear), or mixed (combining the two previous components) [2,3].

The frequency range of humans is not the same as that of the animals, and some sounds, imperceptible to the human ear, may be disturbing to animals. The hearing range in humans goes from 20 to 20,000 Hz, while in dogs is from 15 to 50,000 Hz, cats from 60 to 65,000 Hz, in dolphins goes from 150 to 150,000 Hz and in bats from 1000 to 120,000 Hz [4-6].

A characteristic related to the aging of mammals, which is universal, is presbycusis, defined as the hearing loss associated with advancing age [7,8]. In animals, studies are carried out and, when having a beneficial result, can be applied to humans making possible to discover innovative solutions and treatments for some diseases.

The neurophysiology of tinnitus has been studied and understood through studies with animal models. Tinnitus and hearing loss are two concepts that are closely related [9]. The definition of tinnitus consists of the perception of a sound heard without the presence of any physical sound source, whether external or internal to the body.

Animal models used in research expand the neuroscience of tinnitus and explore cognitive factors, however, only the sensory characteristics of tinnitus were analyzed. In this article, it was not possible to determine whether emotional characteristics can be understood across these animal species. Investigations of sound treatments in animals with tinnitus or hearing loss are negatively rare.

Noise-Induced Hearing Loss (NIHL)

NIHL consists of an injury that occurs at the level of hair cells, which can consequently affect the organ of corti located in the inner ear.

In recent years, many studies related to NIHL in animals have been carried out. For the assessment and treatment of NIHL, the phylogenetic proximity between the scientifically designated nonhuman primates and humans must be considered, given the high similarity of the two auditory systems at the genomic, physiological, anatomical and behavioral level.

Acoustic noise levels in animal facilities, such as kennels, associations or even laboratories, can have harmful effects on animals, regardless of the genetics of each one. In animal research, an acoustic environment with a very high background noise is a factor that is often neglected and is sometimes related to the fact that sound exposure has a negative extra-auditory impact in many species. Prolonged exposure to high-intensity and long-lasting sounds triggers several changes in animals, especially in older ones, and can damage the auditory system permanently.

Hearing tests: Brainstem Auditory Evoked Potentials (BAEP) and Acoustic Evoked Otoemissions (AOE).

BAEP is an objective hearing test that assesses the neuroelectric response of the brainstem. This exam is performed with a click stimulus and can generally be used when the result is “fail” (failure or refer) in the AEO test in animals.

Tests such as BAEP or even Electrocochleography (ECoG) are adapted to be used in animals. The monkey has a wave morphology quite similar to that of humans, with waves I, II and IV being the most prominent (representing the distal and proximal cochlear nerve activity and the superior olivary complex, respectively), because they are better analyzed and reliably obtained in this animal species.

Distortion Product Acoustic Evoked Otoemissions (DPAEO) are the most applied in the veterinary environment, namely when trying to find out which auditory frequencies are most affected. For this reason, are the most used to evaluate species, such as the cat or the dog. Transient Acoustic Evoked Otoemissions (TAOE) can be considered an alternative test where the response to several clicks is indicated.

This systematic review intends to thoroughly examine the existing literature on hearing loss and hearing assessment in animals. The search was carried out on the PubMed and B-on, in January 2023. The search terms used were: “hearing loss AND animals” and “deaf animals” both in the Title/Abstract.

The inclusion criteria applied were the following: vertebrates, birds, land and marine mammals; articles written in English, Spanish and Portuguese; articles with full text access.

The exclusion criteria: Rodents; syndromes and dementias; laboratory-induced hearing loss; Deoxyribonucleic Acid (DNA) studies; drugs, chemicals, pharmaceuticals and iodine deficiency; no full-text access to some articles; systematic reviews and mini-reviews.

The review process was performed according to PRISMA and flowchart is in Figure 1.

 

Figure 1: PRISMA flowchart.

The total number of articles found in PubMed and B-on was 261, with 225 articles being excluded, leaving 26 articles for analysis, as shown in Figure 1.

The countries with published articles are the United States of America (USA; 14 articles), followed by Canada, Japan, Slovenia, Spain, the Netherlands, Germany, Australia, China and Austria. The articles range between the year 1983 and 2022.

The most analyzed species in these 26 articles were the cat (reported in 15 articles), the monkey (in 14 articles), and the dog (in 6 articles), among others. The tests mostly used were the BAEP (reported in 13 articles), electrophysiological recordings or electrical stimulation were also performed (in 8 articles), and the AOE (in 5 articles).

Hearing loss is discussed throughout the articles with the most reported type being sensorineural or unspecified (approached in a total of 13 articles). NIHL follows, or just noise (with a total of 11 articles). Finally, tinnitus is addressed in 10 articles, among other clinical conditions addressed. Table 1 summarizes some information about the articles. This table is divided into six main information analyzed: The author(s) and year of publication, the country, the sample number, species, the equipment and tests to assess hearing, and the final notes.

Table 1: Overview of global animal auditory research, detailing species, methodologies (e.g., ABR, AEP, MEG), and key topics such as hearing loss, tinnitus, cochlear implants, and neuroplasticity.

Many aspects of hearing physiology were first analyzed in animals and only later studied in humans, such as auditory deprivation. With impairment of hearing and balance, visual cues and body language accompanied by verbal commands, make it easier to interpret what is said, thus, the animals studied seem to adapt well to the familiar environment with humans. These sensory deficits can delay the detection of compensatory forms in animals.

Studies analyzed revealed that the facilities/labs where animal’s studies are carried out, have little sound absorption and increased reverberation times. Noise can arise from technical devices such as air conditioners and other equipment, or from the movement of people who take care of the space, from the opening/closing of doors, or even from the animals themselves with their chewing, vocalization, rattles, the tapping of bird cages and communication between them. They can also make more noise in the presence of the employees who work there. The barking and howling of dogs can produce a sound greater than 90 dB SPL, reaching peaks between 105 and 120 dB SPL.

The very high noise in these dwellings can be characterized as a random sound in space. This unnecessary noise can be reduced in animal rooms and corridors using sound absorbing panels. In animal facilities, the acoustic environment and careful monitoring are important to obtain information about sources of noise variability.

Environmental noise disturbs animal behavior very similar to humans, namely maternal behavior, and triggers some changes in animals such as differences in metabolism: Increase in adrenal, uterus and ovary weight, altered tumor resistance and immune response, sleep disturbances, wound healing is slower, cardiac hypertrophy, decrease in body weight, hypertension, infertility, termination of pregnancy, embryonic abnormalities and spontaneous lactation may occur.

Our analysis revealed that hearing loss in cats can be hereditary congenital sensorineural, being the most common, late-onset acquired sensorineural or late-onset acquired transmission. Late on set acquired transmission hearing loss is associated with external and/or otitis media. In turn, late onset acquired sensorineural hearing loss is related to presbycusis or ototoxicity. Moreover, unilateral congenital hearing loss in cats can trigger small changes in the cerebral cortex. Unilateral hearing loss is not detected through behavioral tests as these are subjective. For this reason, do not appear to be very reliable. Cats with white fur and blue eyes are often linked to having genetic hearing loss. Hereditary hearing loss in cats is more common than acquired hearing loss. These losses can be unilateral or bilateral and are more studied in Dalmatian dogs and cats with white fur with one or two blue eyes, cats with two blue eyes have more probability to have hearing loss.

Regarding presbycusis, it can be detected in dogs especially in older ones, through BAEPs. With this test it is possible to detect a progressive hearing loss, with the highest frequencies being firstly affected. In cats rarely happens but can start after adolescence and has a low impact compared to dogs.

For a better diagnosis and treatment, a study was carried out in animals phylogenetically identical to humans. The phylogenetic proximity between non-human primates and humans has the great advantage of including primates in basic biomedical research, since they share about 93.5% of genetic similarity. The primate’s cochlea is about three times smaller than the human cochlea. The species of monkeys Rhesus has a decrease in auditory acuity between the ages of 25 and 31, this information was proven through the BAEP, from which it was verified that the elderly monkeys of this species had smaller wave amplitudes compared to the younger ones.

It is possible that adult animals learn more through classical and/or operant conditioning, habituation, intensive training, or the practice of a sensory task. In classical conditioning, learning takes place through the association of stimuli (involuntary response), while in operant conditioning, learning takes place through positive/negative reinforcement (voluntary response). Habituation is capable of being maintained for several weeks after the elimination of the repetitive stimulus. In turn, conditioning causes a rapid and specific change in the neuronal activity of the auditory cortex.

Regarding tinnitus, there are two types of models applied: Interrogative and reflexive. Interrogative models investigate the auditory experience of animals and analyze how much tinnitus affects them behaviorally in an acoustic environment. Positive reinforcement is also used to stimulate these animals, and punishment as a way of scolding them, verifying that the negative stimulus is the most effective. These models rely on hearing perception, so animals hear and act differently to the same sound. This model can also be used to assess how an animal perceives its tinnitus but requires prior training and motivation, which is a disadvantage for this model. Reflexive models can assess auditory reflex change with tinnitus, characterize the way tinnitus alters unconscious reflexes and depend on these same reflexes that do not require incentive or prior training, as is the case of the acoustic startle reflex. Both models take long periods of time and require very thorough experimental control. Tinnitus also involves cognitive and emotional components and is not considered just a phantom hearing sensation. However, such aspects have not been studied in animals.

Some animal models are trusted to provide an objective measurement of tinnitus and this measurement was developed to help non-verbal individuals. Manganese-Enhanced Magnetic Resonance Imaging (MEMRI) is a very advantageous test that assesses brain function and tinnitus. Moreover, two studies revealed that cochlear implants that are electrically tested in animals and improve the presence of tinnitus. Furthermore, white cats with congenital loss have a degenerated organ of Corti. Auditory pathways are only activated through electrical stimulation from a cochlear implant. In both humans and cats, the effects of using a cochlear implant are similar.

Animal studies seem to vary according to the species (monkeys, dogs, cats, among others), the age of the animal (whether it is newborn, young, adult or old), the types of measurements (either behavioral, anatomical or physiological), deprivation methods (environmental deprivation, tampons or surgical intervention), stimulation methods (click or tone burst stimulus), intensity tested (dB SPL), stimulus frequency (Hz), duration of exposure to sound and, finally, hearing recovery time after auditory deprivation.

The limitations of this study are the fact that some articles do not mention sample sizes, do not describe the species, and the absence of information such as gender and age. More studies could be carried out with specific species of animals.

It is of interest to develop more information on this topic in further studies, helping both humans and animals.

Animal studies are relevant to better understand the biological phenomena of non-induced hearing loss and we can transpose the effects/mechanisms to the human species through theoretical models. It is possible to say that animals also suffer from hearing loss and that they can perform the same tests as humans using different techniques and procedures.

With this review we can conclude that hearing loss affects animals in the functionality of the cardiovascular and endocrine systems, in the auditory system itself and in the vestibular system, although the behavior will be different. Compared to human behavior, animals will be more visually attentive. If the type of loss in animals is sensorineural, it may affect the inner ear and, consequently, the organ of Corti, if it is a transmission loss, it will affect the outer and/or middle ear, and if it is a mixed loss, both anterior components are affected.

This review also revealed that sensorineural and transmission losses are more addressed, however, sensorineural loss is the most recurrent type of loss.

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The authors declare that there is no conflict of interest.

Not applicable.

DN and DT: Conceptualization, methodology, literature search (screening, selecting, and extracting data from studies in review), manuscript original draft, review and editing. DN: Conceptualization, methodology DT: Conceptualization, manuscript review. FC: Conceptualization, supervision. DT and FC: Literature search, manuscript writing, review and editing.

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