Hidden hearing loss

According to the popular opinion, loud voices cause muffled sound or tinnitus in the ears, but the ears soon recover. However, high sound levels can cause permanent damage to the auditory nerve fibers that transmit the sound to the brain. Covert hearing loss can allow the sufferer to hear voices without understanding what the speaker is saying. A drug that allows damaged nerve fibers to regenerate may provide one solution to this common problem.
The article was published with the approval of Scientific American Israel and the Ort Israel network

The fans of the football teams "Seattle Seahawks" and "Kansas City Chiefs" compete with each other at their home games to break the Guinness World Record for the loudest stadium. On October 1, 2014, the Chiefs reached the latest record: 142.2 decibels (dB). This level of noise is similar to the ear-splitting roar of a jet engine at a height of 35 meters, a typical example that hearing experts bring to noise whose intensity is higher than the minimum intensity that causes hearing damage. After the game the fans were ecstatic. They smiled at the experience, and talked about the ringing in their ears and the feeling that their eardrums were about to explode. But what happened inside their ears was not wonderful at all.

If the fans had been given hearing tests before and immediately after the game, they would have noticed a noticeable deterioration. The softest sound a fan could hear before the opening kick, it was said, words spoken in a whisper, would not have caught his ears already at half time. And the threshold levels for hearing would increase by 20 to 30 decibels when the final whistle sounded. With the ringing in the fans' ears a few days after the game, the findings of a hearing test, an audiogram, might have returned to the initial level, because the ability to hear faint sounds would have been renewed.

For a long time, scientists believed that once the hearing threshold returns to its normal level, the ears also recover from the damage caused by the noise. Recently, my colleague and I have shown that this assumption is incorrect. Even exposure to noise that causes temporary damage to hearing may nevertheless cause immediate and irreversible damage to the auditory nerve fibers that carry the information about sounds to the brain. Such damage does not necessarily affect the ability to recognize tones, as seen in the audiogram, but it may inhibit the ability to process more complex signals. This condition, which was recognized recently, is called latent hearing loss because a normal audiogram may miss the damage caused to the nerves and the accompanying hearing impairment.

As people continue to abuse their ears, so does the price charged by hearing sensors. In fact, such damage may contribute to the gradual decline in middle-aged and aging people's ability to distinguish subtleties of speech sounds. However, latent hearing loss does not only affect older people. The newest studies indicate that in an industrial society, hidden hearing loss may appear at younger ages, due to the increased exposure to loud noises, which can be avoided, even if not all.

A wonderful sense organ

The ear's vulnerability stems from its wonderful sensitivity, which allows it to respond to a huge range of sound levels. Our lower hearing limit, the ability to distinguish quiet sound at frequencies close to 1,000 vibrations per second, or 1,000 hertz (Hz), is defined as zero decibels. The hearing index is a logarithmic index, every 20 decibel increase in sound volume corresponds to a 10-fold increase in the amplitude (amplitude) of the sound waves. At zero decibels, the auditory bones in the middle ear, whose vibrations drive the hearing process, move in place to a distance less than the diameter of a hydrogen atom. At the other end of the continuum, such as painful noise intensities exceeding 140 decibels, as achieved by the Chips fans in the record they broke in the football game, the ear has to deal with sound waves whose amplitude is 10 million times higher.

Hearing begins when the outer ear conducts sound waves through the auditory canal to the eardrum which vibrates and moves the auditory bones in the middle ear. The vibrations of the auditory ossicles are transmitted to the cochlea, a fluid-filled canal, coiled around itself in the shape of a cochlea, located in the inner ear. In the cochlear canal is a strip of tissue called the organ of Corti, which contains sensitive sensory cells called hair cells. The cells are so named because of bundles of thin hair-like projections that stick out of them and protrude into the cochlear canal. The thin extensions themselves are called stereo-cilia, and they are soaked in the liquid that fills the cochlear canal. The hair cells most sensitive to high frequencies of sound waves are found at the beginning of the spiral of the cochlea, and those most sensitive to low frequencies are found at its other end. Each hair cell sends out a nerve extension that creates a synapse at its end with one of the fibers of the auditory nerve. When sound waves move the ossicles they create waves in the fluid that bend these "hairs" or eyelashes. The hair cells convert the oscillations into chemical signals and release molecules of a nerve messenger (neurotransmitter) called glutamate from the end of the nerve branch of the hair cell.

The released glutamate passes through the synapse gap between the two nerve cells through diffusion and binds to receptors located in the membrane of an auditory nerve cell. From the other side of the auditory nerve cell comes out an extremely long nerve fiber called an axon. The nerve fibers of all auditory nerve cells together form the auditory nerve. The glutamate that binds to the nerve cell triggers an electrical signal that travels along the nerve fiber and reaches the brainstem through the auditory nerve. From the brainstem the signals progress through a series of parallel neural feedback loops, which spread to different areas of the brain, from the brainstem to the midbrain and thalamus, and end their journey in the auditory cortex. The set of these complex connections analyzes and organizes the environment into recognizable series of sounds, whether it is a familiar tune or a siren's wail.

There are two types of hair cells: outer and inner. Outer hair cells amplify the vibrations induced by the sound waves in the inner ear, while the inner hair cells translate the vibrations into the chemical signals that stimulate the passage of electrical impulses in the auditory nerve. The inner cells are the most directly responsible for what we perceive as "hearing" because 95% of all auditory nerve fibers form synapses only with the inner hair cells. The question of why so few nerve fibers connect the outer hair cells to the brain is a mystery, but it has been hypothesized that nerve fibers connected to the outer hair cells may be responsible for the pain we all feel when the volume approaches 140 decibels.

In the past, hearing loss was measured mainly through audiograms. Ear doctors have known for a long time that a high percentage of metal workers, who ground sheets in the boiler industry, suffer from permanent hearing loss of sounds in the medium frequency range. Audiograms record our ability to hear tones in octave frequency intervals: for example, 250, 500, 1,000, 2,000, 4,000 and 8,000 Hz. In the early stages of noise-induced hearing loss, the audiogram indicates a phenomenon known as the "boiler manufacturers' gap", meaning the inability to recognize sounds in the medium frequencies of the human hearing range.

In the 50s and 60s of the 20th century, epidemiological studies of workers in noisy factories showed a clear connection between the duration of work in the factory and the decrease in hearing acuity. The initial drop of 4,000 Hz tends to spread over time to additional frequencies. Many of the older workers have completely lost their hearing in the frequency range above 1,000 or 2,000 Hz. Such hearing loss of the high tones causes severe hearing impairment because most of the information conveyed in speech is in the frequency range whose reception has been impaired.

Studies such as these in humans encouraged the US federal government in the 70s to formulate guidelines that would limit exposure to noise in workplaces. Today, several federal authorities are working to regulate the intensity of noise in workplaces, including the National Institute for Occupational Safety and Health, and the Directorate for Occupational Safety and Health. But different government agencies offer different noise limits. The lack of clear agreement reflects the challenges that make it difficult to estimate the risk of noise damage. The problems are of two kinds: first, there are huge individual differences in sensitivity to noise. There are those who can be described as having "hard" ears, and in contrast there are those who have "delicate" ears. This means that the makers of the regulations are required to decide what proportion of the population they choose to protect, and what degree of hearing loss can be considered acceptable. The second problem is that hearing impairments occur due to a complex combination of duration, intensity and frequency of the sounds that the person is exposed to.

Today, the Occupational Safety and Health Administration (OSHA) sets an upper limit of 90 decibels in an eight-hour workday. The risk of damage due to noise at levels above 90 decibels is in direct proportion, approximately, to the total energy that reaches the ear (duration multiplied by intensity). For every additional 5 decibels above the eight-hour standard, OSHA guidelines recommend cutting the exposure time in half, in other words, a worker must not be exposed to 95 decibels for more than four hours each day, or to 100 decibels for more than two hours each day. According to these values, the football fans competing for the Guinness record for noise should not be exposed to their record, of 142 decibels, for more than 15 seconds. Of course, OSHA is not in the business of monitoring noise levels on sports fields, or even on US agricultural farms, where teenagers driving tractors and combines for days at a time are at serious risk of hearing loss.

Auditory trauma - following the loud noise: after sound waves pass through the auditory canal, and through the eardrum, they reach the inner ear. There, in the organ of Corti, the sound waves trigger vibrations that stimulate the outer hair cells (within the magnification). These oscillations, amplified by the outer hair cells, are picked up by the inner hair cells, and translated into nerve signals that are transmitted to nerve fibers in the auditory nerve. Destruction of hair cells has long been known to cause hearing loss. But now it turns out that the nerve fibers can also be damaged by loud noise, which leads to hearing loss even if the hair cells themselves are not damaged.

For the past 60 years, audiologists have assumed that routine monitoring using audiograms is enough to reveal all the important information about noise-induced hearing damage. Indeed, an audiogram shows if damage has occurred to the hair cells in the inner ear, and hearing researchers in the 40s and 50s discovered that the hair cells are among the most vulnerable cells in the inner ear when overexposed to acoustic shocks.

Animal experiments, some of which were done in our laboratory, showed that the outer hair cells are more vulnerable than the inner hair cells, that hair cells in the part of the cochlea that detects high-frequency tones are more vulnerable than those in the area that detects low frequencies, and that hair cells that are destroyed do not regenerate. Even before a cell degenerates, loud noise can damage the bundles of cilia that protrude from the cell membranes, and this damage is also irreversible. When a hair cell is damaged or dead, the hearing threshold rises: we must turn up the radio or ask the person speaking to us across the table to raise his voice.

A deeper investigation of damage to the cochlea in humans is delayed because it is impossible to remove the tiny hair cells in a biopsy without damaging them, and it is impossible to obtain images of them in a living person by any known method. The damage associated with noise-induced hearing loss in humans has only been studied in the ears of people who have donated their organs to science, after their death.

The question of whether hearing loss is an inevitable part of the aging process, or whether it is the result of repeated exposures to the hustle and bustle of modern life, remains unresolved, in part because of these limitations, and continues to trouble hearing experts. A particularly intriguing clue was obtained from a study done in the 60s, where researchers looked for groups that lived in particularly quiet environments, such as the Mabaan tribe in the Sudanese desert. The hearing test results of men from the tribe, aged 79-70, were significantly better than those of American men of the same age. Of course, it is impossible to separate based on these findings between the effects of other differences between the members of the groups, such as genetic background or diet.

Deep damage

Recent studies my colleagues and I have done have added a new dimension to the understanding of the dangers associated with overexposure to noise. Scientists and doctors have known for a long time that some of the hearing disorders resulting from exposure to noise are reversible, and some are not. In other words, in some cases the hearing threshold returns to a normal level a few hours or a few days after the exposure, and in other cases the recovery is not complete and the hearing threshold will remain permanently high. Hearing researchers used to believe that if the threshold sensitivity to sounds recovers, the ear itself recovers completely. Now we know that is not true.

The intense explosive sound of fireworks on Independence Day or the roar of the crowd at a football game not only affect the hair cells, they also damage the auditory nerve fibers. We, like other researchers, showed in the 80s that particularly strong noise causes damage to the ends of nerve fibers at the sites of synapses with hair cells. The fiber tips of overexcited auditory nerve cells swell and tear, apparently in response to the release of extremely large amounts of the signaling molecule, glutamate. In fact, excessive release of glutamate has a toxic effect anywhere in the nervous system. The conventional wisdom was that noise-damaged nerve fibers must recover or regenerate after exposure to extreme noise, because the hearing threshold returns to its normal level in ears in which excessive swelling of nerve fiber ends has been found immediately after exposure to noise.

In our lab, we doubted that severely damaged synapses in the ears of an adult are capable of regeneration. We also knew that nerve damage due to noise is not necessarily reflected in normal tests, because animal studies showed already in the 50s that the loss of auditory nerve fibers, without the loss of hair cells, is expressed in audiograms only when the loss reaches extreme dimensions, to the extent of 80% of hearing . It turns out that a dense population of nerve fibers is not necessary to detect a sound when testing hearing in a quiet cell. This is equivalent to repeatedly looking at a digital image of a group of people, each time reducing its resolution. As you decrease the pixel density, the details of the characters become less clear. You can still say that you see people in the picture, but you cannot see who they are. Similarly, according to our hypothesis, diffuse loss of neurons does not necessarily affect a person's ability to distinguish sound, but it may easily reduce their ability to understand speech in a busy restaurant. When we started in the 80s to study nerve damage due to noise, the only way to count the synapses between the auditory nerve and inner hair cells was a method of viewing with an electron microscope a series of sections, a very tedious process that required a year of work to examine the synapses of a few hair cells from a single cochlea.

Twenty-five years later, my colleague Sharon G. Kujawa of the Massachusetts Eye and Ear Research Institute and I were engaged in trying to determine whether a single exposure to noise in young mice was sufficient to accelerate the onset of late-life hearing loss. We exposed the mice to noise designed to cause a temporary increase in the hearing threshold without permanent damage to the hair cells. As expected, the cochleae of the rodents appeared normal a few days after exposure to the noise. But when we examined the animals after six months to two years, we noticed a cumulative loss of auditory nerve fibers, even though the hair cells appeared intact.

Fortunately, since the 80s we have learned a lot about the possibilities of studying the molecular structure of synapses. Today it is possible to bind antibodies to different structures on both sides of the synapse between the inner hair cell and the auditory nerve fiber, and mark them with fluorescent markers. The markers allowed us to count the synapses easily using a light microscope. Soon we were able to collect data that showed that a few days after the noise exposure, when the hearing threshold returned to its normal level, no less than half of the synapses of the auditory nerve disappeared, and did not regenerate. The loss of the rest of the nerve cells, the cell bodies and the axons that reach the brain stem, was discovered within a few months. Two years later, half of the auditory nerve cells were completely gone. Once the synapses were destroyed, the nerve fibers remained dysfunctional and did not respond to sounds with any intensity.

In recent years, we have documented noise-dependent deterioration of synapses in mice, voles and chinchillas, as well as in human tissues examined after death. In animal studies and in human ears, we have shown that the loss of the connection between auditory nerve fibers and hair cells occurs before an increase in the hearing threshold linked to the loss of hair cells is noticed. Today, many accept the idea that damage to the auditory nerve causes a kind of hidden hearing loss and that this damage is an important component of hearing loss due to noise and aging. Many ear doctors and hearing researchers are now developing tests that will test how common the problem is and whether our noisy lifestyles are leading to an epidemic of ear damage in people of all age groups.

nerve repair

In the simplest terms, an audiogram is the standard preferred by all doctors for diagnosing hearing thresholds, and it provides a sensitive test for the destruction of hair cells in the cochlea. However, it is very weak in detecting the destruction of auditory nerve fibers. Our research has shown that the neural damage caused by covert hearing loss does not affect the ability to detect the presence of sound, but it most likely reduces our ability to understand speech and other complex sounds. In fact, it may be a major contributor to the classic complaint of the elderly: "I can hear people talking, but I can't understand what they're saying."

Hearing researchers have known for a long time that two people with similar audiograms can perform very differently on so-called speech-in-noise tests, which test the number of words they recognize as the background noise increases. In the past, these differences were attributed to differences in brain processing. Our research shows that a significant part of the differences is due to differences in the number of auditory nerve fibers remaining after cumulative damage.

Hidden hearing loss may also help explain other common hearing problems, including tinnitus (ringing in the ears) and extreme intolerance to moderate-intensity noises, a phenomenon called hyperacusis. These disorders are present even when the audiogram does not indicate any problem. In the past, researchers and doctors relied on a normal audiogram of a person suffering from tinnitus or hyperacusis and saw it as evidence that the problem was in the brain. We hypothesized that the damage may be in the auditory nerve.

Our research raises questions about the risks associated with routine exposure to loud music at rock concerts and clubs, as well as through personal listening devices. Although noise-induced hearing loss is undoubtedly a problem among professional musicians, and even among those who play classical music, epidemiological studies of casual listeners have not revealed any significant findings in their audiograms. The guidelines of the federal government in the USA, written with the aim of minimizing damage among workers, are all based on the assumption that if the hearing thresholds after exposure to noise return to their normal level, the ears have fully recovered. As we discovered, this assumption is wrong; From this it follows that apparently the current noise prevention rules are not enough to prevent nerve damage due to noise and the hearing damage that accompanies it.

To deal with this problem, we need better tests for diagnosing the destruction of the auditory nerve, which are not limited to counting synapses in the tissues of dead people. One promising approach is based on an existing measurement of electrical activity in auditory neurons called the auditory brainstem response (ABR). This measurement can be performed in an awake or sleeping subject, by attaching electrodes to his head that measure electrical brain activity (EEG) in response to playing bursts of sounds at different frequencies and at different levels of sound pressure. (Sound pressure is the degree of deviation from the atmospheric pressure prevailing in the environment, which causes sound waves.) In the past, it was common to interpret the results of an ABR test in terms of pass or fail: the appearance of a clear electrical response due to sound production was interpreted as normal hearing, and the absence of such a response was considered evidence of damage auditory.

In animal studies we have shown that the amplitude of ABR at high noise levels contains a lot of information: it increases in direct proportion to the number of auditory nerve fibers whose connection with inner hair cells is preserved. At the same time, a recent epidemiological study inspired by our study used a modified version of the ABR test in a group of English college students with normal audiograms, and found lower response amplitudes among those who reported heavy exposure to noise in clubs and rock concerts.

The search for effective treatments for hidden hearing loss raised the question of whether it is possible to repair damage caused by noise by treating the surviving nerve cells with substances designed to encourage the regrowth of nerve fibers, thus enabling the renewal of connections with the inner hair cells. Although the synapses themselves are destroyed immediately after exposure to noise, the slowness of the degeneration process of the other parts of the nerve cell (the cell body and its axon) gives us hope that we can restore them to normal function. We obtained encouraging results in animal studies, using substances that promote the growth of nerve fibers (neurotrophins) that were inserted directly into the inner ear. It may be possible to treat latent hearing loss by injecting through the eardrum a gel that will release slow-release neurotrophins in a way that allows synapses to be restored months or years after the noise impact. They will be inserted immediately after exposure to loud noise, such as the sound of the explosion at the finish line of the Boston Marathon in 2013, which destroyed the hearing of more than a hundred spectators. It is possible that one day an ear doctor will be able to deliver drugs to the cochlea for minimally invasive treatment of damage to the ear caused by noise, as easily as an eye doctor corrects nearsightedness with laser surgery of the cornea.

good to know

How to protect your hearing in a few simple steps

In studies of animals of different species, continuous two-hour exposure to noise with an intensity between 100 and 104 decibels caused irreversible damage to the auditory nerve in the ear. There are good reasons to think that the human ear is just as sensitive. Most exposures to noise in everyday life do not last long. Nevertheless, you should avoid unprotected exposure to sounds above 100 decibels.

Many sounds heard during the day bring us closer to the danger zone. Rock concerts in halls and club music usually produce peak levels of 115 decibels and average levels are above 105 decibels. Leaf blowers and lawn mowers reach the user's ears at levels of 95 to 105 decibels, as do devices with motors such as circular saws. The frequency of the sounds is also important. The louder the growl of a sanding belt, the more dangerous it is than the low-toned roar of an unmuffled motorcycle, even if at the same decibel level. Air hammers produce a noise reaching 120 decibels even to the ears of a person passing by at random, and the rapid tapping of the metal rod on concrete produces a lot of high-pitched sounds that are dangerous to the ears.

what can we do? Today many of us have access to incredibly accurate noise meters in our pockets or purses. There are many cheap or free applications adapted to phones with the Android operating system or to Apple iPhones, which provide reliable measurements of sound pressures produced by musical instruments or the roar of a motorcycle leaping from the spot, with a level of accuracy that hardly falls short of that provided by professional sound control equipment from the most expensive. The iOS-compatible app that worked great for me, Sound Level Meter Pro, costs less than $20 and has accurate readings of less than 0.1 decibels.

The good news is that once you find out which noises in the environment may endanger your hearing, you can use effective ear protection measures, which are cheap, easy to obtain and very convenient to carry from place to place. Stiffened foam earplugs, if inserted correctly, can moderate sound volume by 30 decibels in the most dangerous sound frequency areas. Roll such a gasket between your fingers and shrink it into a roll as thin as you can, and quickly thread it as deep as possible into the sound canal. It is no more difficult or dangerous than using a small headset or headphones that sit on the head. Let them expand slowly, and a minute later you're ready to tear up the club with all that rock.

If you're listening to a rock performance, these foam plugs muffle the sounds excessively. If you want to hear the sounds, but at a lower volume, use a "musician's headset". There are different types available for purchase online for $10-$15 per pair. They are designed to moderate the volume at the level of 10-20 decibels, and dim the low and high tones equally, so that the overall tone of the music is not affected.

And most importantly, pay attention to what your ears are telling you. If you leave an event or activity with the feeling that voices sound muffled, as if you have cotton wool in your ears, or if you hear ringing in your ears, there are many chances that you have destroyed some synapses of the auditory nerve cells. Do not despair, but do not repeat the mistake.

About the writers
M. Charles Lieberman Professor of Otology and Laryngology (throat problems related to the voice) at Harvard Medical School and Director of the Eaton-Peabody Laboratories at the Massachusetts Eye and Ear Institute. He is an expert in researching the pathways between the inner ear and the brain.