Download Hyperesthesia: An Integrative Review

Introduction
Because areas of knowledge are fragmented, potentially useful
information in one field may go unnoticed by researchers in other related, but
non-communicating fields of study. This is especially true for medical
knowledge. Swanson (1990) observed that such fields of study are noninteractive or mutually isolated. Undiscovered relationships between noninteractive bodies of literature, according to Swanson, can be exploited to
generate new theories about etiology or treatment for different conditions. One
of the ways in which complementary fields of literature may be linked is through
the common causes of different conditions.
There are many terms for hypersensitivity to sensory stimuli.
Hyperesthesia (Head, 1929) and sensory defensiveness (Knickerbocker 1980)
both refer to intolerance for sensory stimuli. People with hyperesthesia or
sensory defensiveness may react negatively to normally benign light, sound,
touch or temperature. Hyperacusis is a lowered threshold of discomfort for
sounds. In photophobia, normal intensities of light are painful.
This paper will describe different types of hypersensitivity to sensory
stimuli. It will also describe a possible common underlying cause for some cases
of this oversensitivity and investigate whether diagnostic or therapy techniques
for sensory defensiveness, hyperesthesia, hyperacusis or photophobia, used
with a variety of participant populations, may be useful for people with traumatic
brain injury (TBI).
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Early Descriptions of Hyperesthesia
Hyperesthesia was observed by Henry Head (1929) in patients with spinal
cord injuries and brain injuries. Initially, these patients showed elevated
thresholds for tactile sensation. With the partial return of feeling some of these
patients developed more vivid sensations of pressure, pinprick, heat and cold.
Sensitivity to temperature and roughness affected eating. One participant, who
suffered a stroke, said “food always seems rough and cold” on the affected side.
In addition to touch and temperature, Head’s participants exhibited aversive
responses to sound.
Head believed that the thalamus was responsible for establishing the
“feeling tone” of different sensations. Subcortical lesions disrupted connections
between the thalamus and cortex. He attributed exaggerated responses to a
loss of cortical control over sensory stimuli.
Riddoch (1938) noted that pain from thalamic lesions was often
exacerbated by loud noises and bright lights. Extremes of heat and cold also
caused pain. For one of his patients cold water, applied to the affected side,
produced a “shock, like electricity”. Even a drop of rain on the participant’s left
hand provoked a violent reaction. Pain often radiated throughout the affected
side of the patient’s body. Strong smells or tastes sometimes elicited pain,
though not as often as other types of stimuli.
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Sensory Defensiveness
A. Jean Ayres (1972), citing Head’s (1929) description of hyperesthesia,
used the term tactile defensiveness to describe a developmental disorder.
Ayres, an occupational therapist, observed that people with congenital disorders,
such as autism or mental retardation, were often tactilely defensive; they reacted
negatively to light touch on their face, arms or legs. Hypersensitivity to hot or
cold was also common. Because of these problems, people with tactile
defensiveness avoided certain activities of daily living, such as showering,
washing their face or cutting their nails (Fisher et al. 1991).
Knickerbocker (1980) used the term sensory defensiveness to describe a
condition in which other sensory modalities, such as audition, vision, olfaction or
taste, not just touch elicited aversive reactions. Sensory defensiveness was
reported among children with cerebral palsy and hemiplegia (O’Malley and
Griffith, 1977) as well as people who were developmentally delayed or autistic
(Barenek et al. 1997).
Dunn (2001) pointed out that people who were sensitive to one type of
sensory stimuli often reacted defensively to other types of input. She and other
occupational therapists developed sensory integration rating scales (Dunn 2001,
Brown et al. 2001). . Sensitivity to sensation was one dimension on that scale.
People with autism, for example, were rated by others as having significantly
different responses to touch, light sound, etc. than control participants. Dunn
(2001) also advocated using her scale to study people with traumatic brain injury
(TBI).
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Miller et al (1999) measured electrodermal responses (EDR) to sensory
stimuli in participants with Fragile X syndrome. EDR reflected reactions of the
sympathetic nervous system (SDS) to threatening or startling stimuli.
Participants with Fragile X syndrome showed significantly greater responses to
olfactory, auditory, visual, tactile and vestibular stimuli than did control
participants.
Davies and Gavin (2007) used electroencephalography (EEG) and Event
Related Potentials (ERPs) to compare the responses of children with impaired
sensory processing, as classified by the Sensory Profile, motor skill assessments
and clinical observations, with a control group of children who were developing
typically. The authors measured participants’ responses to pairs of auditory
clicks. These responses, resulting in a positive deflection on EEG 50
milliseconds post stimulus (P50), evaluated the ability of participants’ brains to
filter repeated stimuli. Reduced amplitude to the second click of the P50
indicated intact sensory gating. The authors found that children with impaired
sensory processing showed less sensory grating than the control group, although
the differences were not statistically significant.
Alexander (1987) noted that infants and children with cerebral palsy often
had difficulty tolerating tactile sensation that was light, fast, and poorly graded.
When applied to the face or mouth, such sensation led to defensive reactions,
such as tonic bite reflex and tongue retraction. These defensive reactions
hindered feeding and oral cares. Children who were hypersensitive to taste,
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texture, smell or temperature might exhibit food or liquid selectivity (Bahr 2001),
rejecting all but a few types of food.
Photophobia
Intolerance for light, or photophobia, may be caused by damage to the eye
itself. Bacotti (2001) noted that ocular causes of photophobia included corneal
scratches, cataract surgery, dry eye syndrome, glaucoma, macular degeneration
and diabetes. Conditions such as migraines, tumors and intracranial
hemorrhages were causes of non-ocular photophobia.
Cummings et al. (1981) described a patient who exhibited intolerance to
light after right occipital and thalamic infarctions. Three months after a right
posterior artery occlusion, he demonstrated unusual sensitivity to bright lights.
The authors described this condition as central dazzle rather than true
photophobia because the patient found bright light to be merely disagreeable not
painful.
Hyperacusis
Dubby, Sinks, and Pterein, (2000) found that people with hyperacusis
perceived as painful sounds that were at a comfortable level of loudness for
people with normal hearing. Marriage and Barnes (1995) differentiated between
central and peripheral hyperacusis. Peripheral hyperacusis could be caused by
the loss of the stapedial or acoustic reflex and was therefore associated with
Bell’s palsy, Ramsey Hunt syndrome and myasthenia gravis. Sensory hearing
loss with recruitment was also associated with peripheral hyperacusis.
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Neurological conditions associated with central hyperacusis included
migraine, depression, benzodiazepine dependence, pyridoxine deficiency,
musicogenic epilepsy, Tay Sach’s disease, post-traumatic stress syndrome and
chronic/post-viral fatigue syndrome. Tinnitus and photophobia frequently
accompanied hyperacusis, further suggesting a central etiology. Similarly, Gopal
et al. (2000) observed that a patient with hyperacusis also experienced
hypersensitivity to touch and light. Marriage and Barnes (1995), noting that
disturbed serotonin function was common to each of these neurological
conditions, theorized that a serotonin deficiency was linked to hyperacusis.
Hyperacusis was also found in individuals with William’s syndrome (Klein
et al. 1990, Meyerson and Frank 1987, Nigam and Samuel 1994). In fact, 95%
of people with Williams’s syndrome exhibited hyperacusis (Nigam and Samuel
1994). William’s syndrome is a genetic disorder characterized by infantile
hypercalcemia, supralvular aortic stenosis, mental retardation and distinctive
facial features (Meyerson and Frank 1987).
Hypersensitivity and TBI
There has been a limited amount of research concerning hypersensitivity
to stimuli in persons with TBI. Bohen et al. (1991, 1992) noted that individuals
who suffered post-concussive syndrome exhibited visual and acoustic
hyperesthesia. Their participants reported discomfort at lower levels of
luminance and sound intensity than people without brain injuries. Waddell and
Gronwall (1982) also studied individuals with post-concussive syndrome. Their
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participants were more sensitive than persons without brain injuries to light and
sound. Only differences in tolerance for light, however, achieved statistical
significance. Jackowski et al. (1996) described participants who complained of
photophobia following TBI. Outdoor, fluorescent and bright light sources were
listed as causes of discomfort. Participants also had difficulty reading due to
reduced letter contrast sensitivity. Padula, Argyris and Ray (1994) listed
photophobia as one of a cluster of symptoms that could affect vision after TBI.
Arciniegas et al. (1999) used EEG to study P50 waveforms of evoked
responses to paired auditory stimuli by three participants with TBI. All three
showed reduced sensory gating for auditory stimuli. They also showed reduced
concentration in noisy environments. The authors suggested that TBI, by
reducing acetylcholine available to the hippocampus, might reduce sensory
gating. This disruption in the ability to filter stimuli might contribute to impaired
memory and attention.
The Rivermead Post Concussion Symptoms Questionnaire (RPQ)
included light and noise sensitivity among the symptoms measured by the scale
(Potter et al. 2006). As with other post-concussive symptoms in Chan’s (2001)
study, increased sensitivity to light and noise was also reported by participants
without a history of brain injury. Based on his findings, Chan recommended that
self-report checklists not be used exclusively to diagnose post-concussive
syndrome. He advocated that self-reports of symptoms should be part of a
broader assessment.
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Fluharty and Glassman (2001) described a client with severe brain injury
who reacted aversively to touch, loud noises and extremes of hot or cold. The
client struck out at people who touched him unexpectedly or who made loud
noises. He refused to participate in Activities of Daily Living (ADLs), such as
showering or brushing his teeth, which subjected him to uncomfortable
sensations. He frequently complained about the taste of foods and refused to
eat many items on his tray.
Gilmore et al. (2003) presented a case study of a man post severe
traumatic brain injury who exhibited oral-facial hypersensitivity. The participant
exhibited reduced oral movements due to abnormal tone. These problems
limited oral movement and sensation. Defensive reactions to attempted oral
hygiene included jaw clenching, reflex biting lip pursing and facial grimacing.
Brown et al. (1992) also noted that individuals with closed head injuries
(CHI) often exhibited hypersensitivity to oral and facial stimulation. They
described a patient with a CHI who showed increased muscle tone when
anything was placed in his mouth. He also exhibited severe dysphagia and a
bite reflex. Complicating these problems was the fear and anxiety elicited by oral
stimulation. The patient’s affective reaction further increased muscle tone. Not
only was the client unable to eat, he could not even tolerate oral stimulation
during speech therapy.
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Habituation
The descriptions of hyperesthesia, sensory defensiveness, central
photophobia and hyperacusis exhibited similar features. There might be some
undiscovered implicit, logical connection between the literatures and some
shared condition. Habituation might provide such a connection.
According to Kazdin (2000), habituation is “a decrement in response as a
result of repeated stimulation”. People may be hypersensitive to sensory stimuli
because they do not habituate to repeated stimuli. Since people who are
hypersensitive to sensory stimuli are unable to filter the barrage of sensations
from everyday life, the sensations overwhelm them.
Impaired habituation has been posited as an underlying mechanism in
sensory defensiveness (Reisman and Gross, 1992). Similarly, the nervous
systems of people with central hyperacusis may fail to habituate to startle
responses (Dubby, Sinks, and Peterein, 2000). Central hyperacusis may be
linked to impaired serotonin metabolism (Phillips and Carr, 1998). According to
this theory, neural systems may use serotonin to inhibit and modulate central
nervous system responses to sensory input. Central auditory nuclei receive input
from serotonergic systems.
Implications
Dunn (2001) pointed out that individuals who are sensitive to one type of
sensory stimuli are often defensive toward other modalities. She developed
sensory integration rating scales for both adults and children. Although
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normative data has so far focused on the normal variation of unimpaired
populations (i.e. college students and their relatives), Dunn plans to study special
populations of adults, including those with traumatic brain injury.
If hypersensitivity in one sensory modality increases the likelihood of
hypersensitivity in other modalities, that fact would have clinical implications:
professionals who see patients who are hypersensitive to one type of sensation
(i.e. sound, vision, touch) might want to test or refer patients for testing and
treatment for other sensory modulation problems. Audiologists studying or
diagnosing people with hyperacusis might supplement tests of hyperacusis with
questions about the participant’s ability to tolerate other sensory stimuli. Arani
(1999) did this and found that hyperacusis was often accompanied by
hypersensitivity to light, touch, balance, smell or taste. An ophthalmologist, who
discovered that a patient with photophobia was also hypersensitive to sound,
might refer that patient to an audiologist.
Descriptive questionnaires, (Potter et al. 2006, Dunn 2001) might provide
information to improve understanding of the condition or suggest compensatory
techniques. Clinically, professionals who see patients hypersensitive in more
than one sensory modality might want to refer the patients to others who could
treat the condition affecting that modality.
Neuropsychologists often must perform examinations, particularly
in forensic cases, in which sensory hypersensitivities may confound test results
and represent adverse co-morbid interactions that need to be understood
separately and in relationship to cognitive and emotional factors.
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Sensory hypersensitivity is cited as one among a number of physical
factors including headache and other pain (especially when it becomes chronic),
fatigue and sleep disturbance, sensory loss, and dizziness, related to the head
but not the brain injury, which can directly or indirectly influence functional
outcome (Kay et al, 1992). Even without symptoms of sensory hypersensitivity,
patients frequently complain of distractibility and difficulty attending to more than
one thing at a time.
Treatment approaches that improve habituation for one type of disorder
might improve habituation for other types of disorders. Improved habituation, in
turn, might improve the ability of people with sensory disorders to integrate
sensory information.
Miller et al. (1999) noted higher EDR, which is increased sensitivity to
sensation, among children with Fragile X syndrome in their study who were not
taking medication. In this group of 25 children, 68% of the participants were
receiving medications: 10 received selective serotonin reuptake inhibitors, 3 were
given stimulants and 2 received anti-convulsants. The authors suggested that
future research should investigate the effects of medication on responsiveness to
sensory stimuli.
Gopal et al. (2000) described the effects of selective serotonin reuptake
inhibitors (SSRIs) on the habituation for sound of a participant with hyperacusis,
depression, and hypersensitivity to touch, pressure and light. The participant, as
well as her younger sister, had a history of hypersensitivity to sensory stimuli.
The authors measured auditory responses, including pure-tone threshold testing,
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uncomfortable loudness level testing and auditory brainstem responses (ABRs)
in the participant. Treatment increased the participant’s ability to habituate to
repeated auditory stimuli, as measured by her auditory brainstem responses
(ABRs). Selective serotonin reuptake inhibitors raised the threshold for
uncomfortable loudness levels, indicating greater tolerance for sound. Increased
amplitudes of ABRs in the unmedicated condition may have indicated reduced
habituation to sound. The participant also reported, with administration of SSRIs,
increased tolerance of everyday sounds, bright lights, and touch. An earlier
prescription of imipramine, a tricyclic anti-depressant had not alleviated her
symptoms.
In contrast, Carman (1973) found that the mood of individuals with both
hyperacusis and depression improved following treatment with imipramine. This
group showed greater improvement in affect than did the auditory-normal group
of depressed patients. The author hypothesized that both hyperacusis and
depression were symptoms of central serotoninergic hypoactivity in this subgroup
of patients. He did not report whether hyperacusis improved with drug treatment.
Cummings and Gittinger (1981) found that drug treatment with
amitriptyline hydrochloride, a tricyclic antidepressant, and perphanazine, a
tranquilizer, reduced their patient’s sensitivity to light. The patient had right
occipital and thalamic infarctions. Sensitivity to light diminished with initial drug
treatment but then returned when this treatment was discontinued due to acute
urinary retention. Following transurethral prostatectomy for benign prostatic
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hypertrophy, drug therapy was reinstituted and the patient’s sensitivity to light
diminished again.
Arciniegas et al. (1999) suggested that cholinergic medications might
improve sensory gating for persons with TBI. In additions, such drugs might
improve attention and memory. The authors point out that studies need to be
conducted to determine whether drugs that augment cholinergic function, such
as donepezil, improve sensory and cognitive function in TBI. They suggest that
EEG studies might provide a marker of sensory gating for this population.
Ayres (1972) recommended giving people with tactile defensiveness a diet
of sensory stimulation. This diet was designed to stimulate participants’ higher
cortical centers, thereby helping them integrate threatening tactile input with
knowledge about the situation as well as other sensations. This integration, in
turn, would let participants recognize the seemingly threatening input as
harmless.
Occupational therapists have observed beneficial effects with sensory
integration treatment. Deep pressure, designed to facilitate habituation,
increased participants’ tolerance for other types of stimuli. Studies of sensory
integration techniques have reported generalized improvements in the sensory
modulation abilities of an adult (Reisman and Gross 1992) and children (Miller,
Coll, and Schoen, 2007, Stagnitti, Raison and Ryan, 1999).
Alexander (1987) reported that deep pressure, applied to the sides and
biting surfaces of the gums and teeth may reduce tonic biting reflex for children
with cerebral palsy.
Gilmore et al. (2003) described a desensitization program
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for a client with oral-facial hypersensitivity following traumatic brain injury. Touch
was first applied distally, on the participant’s hands and shoulders with the
therapist’s hands. Desensitization then progressed to neck, forehead, head and
the area around the mouth. As the client tolerated tactile input, the therapist
moved proximally. Stimulation within the mouth, of the teeth, palate and tongue,
was provided by an oral sponge, toothbrush or electric toothbrush. The authors
found that a 2 week desensitization program reduced defensive reactions,
including a bite reflex. These changes allowed the client to participate in oral
hygiene and eat yogurt or thickened liquids.
Brown et al. (1992) described a systematic desensitization program in
which a psychologist helped a patient establish a hierarchy of potentially
threatening types of oral stimulation. The patient began by imagining situations
about which he was slightly fearful, such as a nurse bringing him food. While
relaxed, he alternated between thinking about neutral situations and ones about
which he was anxious. Using this procedure, he was able remain relaxed while
imagining more extreme scenarios, such as a tongue blade touching the back of
his mouth or a choking episode. This program, combined with oral stimulation
by a speech-language pathologist, helped the patient tolerate oral feeding.
Bahr (2001) presented a similar desensitization program for reducing oral
hypersensitivity for children and adults with impaired sensory integration,
including people with traumatic brain injury. She described an oral massage
sequence that, like Gilmore’s (2003), proceeded from distal to proximal
structures. Bahr (2001) suggested using oral massage (Nuk) brushes or oral
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sponges to provide deep pressure to the oral structures. These structures
included the lips, gums, teeth, hard palate and tongue as well as the inner portion
of the cheeks.
Bahr (2001) also described a protocol for increasing food tolerance for
clients with food and liquid selectivity. Therapists would note which foods were
accepted or rejected by clients. They would also note the temperature, taste,
temperature and smell of foods which the client tolerated. This data would be
used to generate lists of new foods to try. Starting with foods possessing
qualities acceptable to the client, the therapist would gradually introduce the
client to a greater variety of foods.
Tinted lenses, prescribed by ophthalmologists, may help people with
photophobia cope with hypersensitivity to light. Jackowski et al (1996) found that
light filtering lenses improved by 39% the reading rate of participants with
traumatic brain injury and photophobia. The reading rate of participants without
brain injury was unaffected by the lenses.
Another approach to ameliorating the effects of inability to tolerate
sensations is to modify the environment to reduce the frequency and intensity of
aversive stimuli. In Fluharty and Glassman’s (2001) case study of an adult with a
traumatic brain injury, intolerance for touch and noise was minimized by
changing his daily routines. Resistance to bathing, for example, was improved
by having the client take baths instead of showers. The fact that taking a bath
did not involve pinprick sensations with extremes of hot or cold temperature
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made it less offensive to the client than showering. Providing distraction in the
presence of loud noises made them less likely to elicit aggressive responses.
Meyerson and Frank (1987) described a desensitization program for a
client with William’s syndrome. Tape recording aversive sounds, then playing
them back with gradually increasing loudness, increased a client’s ability to
tolerate them. A similar approach could be used for clients with traumatic brain
injury.
Jastreboff and Jastreboff (2000) described a program, Tinnitus Retraining
Therapy (TRT), to ameliorate hyperacusis and tinnitus. Their program included
the use of sound generators to facilitate habituation. Sound levels were initially
set near the threshold of hearing then gradually increased. The authors also
emphasized the importance of avoiding the overuse of ear protection: reducing
auditory input increased the hyper-sensitivity of the auditory system. In fact,
gradually enriching the sound environment of individuals with hyperacusis helped
them tolerate sound.
One of the benefits of exploring complementary literatures is that it generates
testable hypotheses. Among the theories for people with TBI generated by
comparing literatures of sensation are the following:
1. Hypersensitivity to sensation, as measured by rating scales, will correlate
with measures, such as, Galvanic Skin Response or Evoked Potentials.
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2. Threshold of discomfort tests such as those employed by Bohnen et al.
(1991) will also correlate with rating scales and with other instrumental
measures.
3. Intolerance for one type of sensation, if caused by central nervous system
damage, will increase the likelihood that hypersensitivity to other types of
sensory stimuli will be present.
4. Treatments designed to increase habituation will ameliorate sensory
hypersensitivity. These might include drug treatments, such as the use of
SSRIs or cholinergic medications, or behavioral approaches.
It should be emphasized that the above are hypothesis and await further
experimental evidence. Much of the research regarding hypersensitivity to
sensory stimuli has focused on populations with specific types of hypersensitivity
among people with diverse etiologies. Additional research is needed on the
incidence of hypersensitivity among people with TBI. It would also be helpful to
study sensory disorders longitudinally to determine if they change as the severity
of participants’ other deficits lessen.
At the present time, client reports of photophobia or hyperacusis are
frequently attributed to desire for compensation or pre-injury adjustment issues
(Lishman, 1988). Instrumental or psychophysical measures might help resolve
controversies surrounding forensic aspects of hypersensitivity. Data from
instrumental tests might complement participants’ reports of symptoms.
Different types of assessments, such as symptom questionnaires, behavioral
observations, physiological and threshold of discomfort tests might provide
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complementary windows into hyperesthesia. Using a variety of measures to
assess sensation could result in a better understanding of hyperesthesia in
traumatic brain injury.
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