Binocular and Accommodative Problems Associated With Acquired Brain Injury
The treatment of binocular vision, accommodative, and eye movement disorders related to acquired brain injury (ABI) is one of the more challenging aspects of optometric practice. Patients who survive ABI generally experience multiple problems, including cognitive, psychological, motor, and sensory anomalies. Even when binocular vision, accommodative, and eye movement problems occur in isolation from cognitive and psychological issues, they tend to be complicated. Cyclovertical and noncomitant deviations, sensory fusion anomalies, unequal accommodation, and visual field loss may accompany the basic vision disorder.
The objective of this chapter is to review the diagnosis and treatment of the most common nonstrabismic binocular vision, accommodative, and eye movement disorders associated with ABI. The emphasis is on determining the various factors that should be considered to determine the potential effectiveness of treatment. As in previous chapters, a sequential treatment approach is presented, allowing clinicians to treat these conditions in an organized manner. We also use a series of cases to demonstrate some of the important concepts discussed in this chapter.
This chapter is not intended to be a complete discussion of all vision problems associated with brain injury. In regard to mild traumatic brain injury (mTBI), Ciuffreda and colleagues1,2,3 have established a conceptual model of optometric vision care that includes four components: (1) the basic optometric examination (acuity, refractive error, eye health); (2) oculomotor-based vision problems (versions, accommodation, vergence); (3) non-oculomotor-based vision problems (abnormal spatial localization, motion sensitivity, photosensitivity, vestibular dysfunction, visual field defect, visual information processing); and (4) non-vision-based problems (depression, cognitive impairment, behavioral problems, postural problems, attentional problems, neurologic problems). This chapter only includes a discussion of oculomotor-based problems.
Overview of ABI
ABI is generally used to refer to both traumatic brain injury (TBI) and stroke or cerebrovascular accident (CVA).
TRAUMATIC BRAIN INJURY
Thurman et al4 define TBI as an occurrence of injury to the head that is documented in a medical record, with one or more of the following conditions attributed to the head injury:
Observed or self-reported decreased level of consciousness
Amnesia
Skull fracture
Objective neurologic or neuropsychological abnormality
Diagnosed intracranial lesion
TBI may result in significant impairment of an individual’s physical, cognitive, and psychosocial functioning.
Up to 2.8 million TBIs occur annually in the United States.5 A significant majority occur in children ages 5 to 18 years, with the highest incidence among adolescents.6,7 Although most appear to fully recover from concussion within 2 to 4 weeks, a subset have prolonged symptomatology affecting their daily function.8,9,10,11,12,13 Over 1.5 million Americans suffer nonfatal TBIs each year that do not require hospitalization.4,14 Another 300,000 individuals suffer brain injuries severe enough to require hospitalization, with 99,000 resulting in a lasting disability. A total of 56,000 people die each year as a result of TBI.4 The prevalence of TBI is estimated to be 2.5 to 6.5 million individuals.15
The number of people surviving TBI has increased significantly in recent years, which is attributed to faster and more effective emergency care, quicker and safer transportation to specialized treatment facilities, and advances in acute medical management. TBI affects people of all ages and is the leading cause of long-term disability among children and young adults.
Individuals aged 15 to 24 years have the highest risk of TBI,4 and TBI affects males at twice the rate that it affects females. In addition, the mortality rate is higher among males, suggesting that males are more likely than are females to suffer severe injuries.4
Although the largest group of TBI survivors are young adults in their prime working years, many survivors, particularly those with a severe TBI, do not return to work. Estimates of those who do not return to work vary widely, ranging from a low of 12.5% to as high as 80%. The ability to return to work is highly correlated with the postacute functional limitations of the survivor.16,17
The severity of TBI is classified as mild, moderate, and severe.18 mTBI is a very common injury, as noted earlier and the term concussion is often used interchangeably with mTBI.19 Many more people are believed to sustain mTBI, but they do not require hospitalization. As a result, an accurate estimation of the number of mTBI cases per year is not available. About 80% of the people admitted to hospital with the diagnosis of TBI have mTBI.20 In a prospective study of 100 consecutive patients, Master et al reported that 69% of their sample of children and adolescents had concussion-related oculomotor problems.13 The most common vision problems found were accommodative disorders (51%), convergence insufficiency (49%), and saccadic dysfunction (29%).13 Hellerstein, Freed, and Maples21 studied the vision characteristics of patients with mTBI and found significant differences between the TBI group and age-matched non-TBI patients. They concluded that the term mTBI is very misleading and does not necessarily translate to “mild functional loss.” This is very significant because most of the optometrists in private practice primarily encounter patients with mTBI. The more severe injuries require hospitalization and various types of rehabilitative therapy. Once the patient enters this system, he/she tends to receive eye care from ophthalmologists. The patient with mTBI, however, will most likely return to the family optometrist if visual symptoms occur after the TBI.
STROKE (CEREBROVASCULAR ACCIDENT)
Stroke, or CVA, is a clinically defined syndrome of rapidly developing symptoms or signs of focal loss of cerebral function with no apparent cause other than of vascular origin, but the loss of function can at times be global.22 The syndrome varies in severity from recovery in a day to incomplete recovery and from severe disability to death.22 Stroke cases can now be classified in epidemiology studies by type. Wolf, D’Agostino, Belanger, and Kannel23 reported that, in the Framingham study, 45% of strokes were classified as atherosclerotic, 19% as cerebral embolism, 19% as transient ischemic attack, 5% as intracerebral hemorrhage, 4% as subarachnoid hemorrhage, and 2% as other, for men aged 55 to 84 years.
Stroke is the third leading cause of death and the leading cause of chronic disability in the adult population of the United States.24 Every year, more than 795,000 people in the United States have a stroke25 and about 610,000 of these are first or new strokes.25 There are about 3.5 to 4 million survivors of stroke.23 Of these survivors, about one-third have mild impairments, another one-third are moderately impaired, and the remainder are severely impaired. CVA can occur at any age, but it is much more common in the elderly. The death rate doubles every 10 years between the ages of 55 and 85.24 The incidence of stroke varies with location. For example, the incidence has been reported to be as low as 238 per 100,000 in Dijon, France, whereas it is 362 per 100,000 in Rochester, Minnesota, and 627 per 100,000 in Novosibirsk, Russia.22 In the United States, there have been consistently higher rates of stroke in the southeastern states since the 1930s.26 With the aging of the population, it is likely that CVA will become even more common in the future. Given the high prevalence of vision problems after CVA, optometrists have an important role to play in the vision care of this population.
Optometrist’s Role
Vision problems are common after ABI, and they have a significant negative impact on common activities of daily living, such as reading, writing, shopping, dressing, sports, and driving.21 Historically, optometrists have not been part of the rehabilitation team in hospitals.27 This team typically includes various physicians and rehabilitation professionals, such as occupational, physical, and recreation therapists and speech/language pathologists. Eye care is usually provided by an ophthalmologist, with a primary emphasis on visual acuity and eye disease.28 As a result, it is common for some vision problems associated with ABI to be left undetected or untreated, leaving the patients with significant functional problems.28,29,30,31,32
In the past decade, however, optometrists have become more involved in the management of vision problems associated with ABI.21,27,30,31,33,34,35,36,37,38,39,40,41,42,43 The optometrist’s role includes management of refractive error; binocular vision, accommodative, and eye movement disorders; visual field loss; ocular disease; and other visual manifestations of ABI. Because of the complexity of ABI, it is important for optometrists to work closely with the rehabilitation team. The nature of this interaction varies with the time frame after the ABI.
ACTIVE REHABILITATION STAGE
During the active rehabilitation stage, it is critical for the optometrist to work closely with the occupational, physical, and speech therapists. Because of the high prevalence of vision problems after ABI, these rehabilitation specialists often encounter patients with vision problems that interfere with the rehabilitation process. Optometrists with staff privileges and working as consultants at these facilities can provide an important service by identifying and managing the vision problems of patients with ABI in a timely manner. During the early phases of rehabilitation, passive treatment (lenses, prism, occlusion) is often prescribed to make the patient as comfortable as possible during rehabilitation. The optometrist should also educate the rehabilitation team about the nature of the vision problems. This education should include information about the effect of these problems on various activities of daily living and how the therapists can modify the environment and tasks to enable the patient to function most effectively.
During this period of time, it is difficult for the optometrist to perform active vision therapy. However, some optometrists do prescribe active vision therapy to be administered in the rehabilitation hospitals by occupational therapists.44 In such a scenario, the optometrist identifies the problem, prescribes and programs the active vision therapy, supervises the therapists who perform the vision therapy, and performs periodic reevaluations. When the active phase of rehabilitation ends and the patient returns home, the optometrist can take full control of the patient’s functional vision care. The active vision therapy program would then continue at the optometrist’s office.
POSTREHABILITATION STAGE
Other scenarios are also possible. Because the majority of optometrists do not have staff privileges at rehabilitation hospitals, they will more likely be involved with ABI patients who have not required hospitalization (mTBI) or patients who have completed active rehabilitation. In other instances, the optometrist may not have the opportunity to examine the patient with ABI for months or even years after the problem occurs. The patient may turn to the optometrist as a last resort. Often the patient may have already visited a number of ophthalmic practitioners and been told either that there is no problem or that treatment is not possible.28,29,31,32 In such situations, the optometrist is the primary caregiver and the sequential treatment approach described in this chapter becomes applicable. If the patient has recently been discharged from a rehabilitation facility, close cooperation with the patient’s therapists will still be important.
Ciuffreda et al29,31 summarized the potential role that optometrists should play in the treatment of ABI patients:
The provision of full-scope optometric care to this underserved and poorly understood clinic population offers a unique and altruistic opportunity for the profession. By such a comprehensive approach, in conjunction with other members of the rehabilitative team, patients with TBI can more rapidly reenter society and the work force, and once again be productive members of the community.
Common Binocular Vision, Accommodative, and Eye Movement Disorders Associated with ABI
BINOCULAR VISION DISORDERS
The common nonstrabismic binocular vision disorders described in previous chapters are often associated with ABI. Cyclovertical heterophoria (Chapter 14) occurs more often after ABI than in the general clinical population. In addition, we sometimes encounter a binocular vision problem called sensory fusion disruption syndrome, which seems to be unique to ABI.45,46,47 Sensory fusion disruption syndrome is a condition in which there is only a small heterophoria, yet the patient is unable to fuse images even though they are aligned bifoveally under optimal conditions.45 This inability to fuse is similar to the strabismic entity referred to as horror fusionis. The prognosis in such cases is usually poor. Treatment with lenses, prism, vision therapy, or surgery is generally unsuccessful, although there have been case reports45,47 suggesting that some of these patients will regain fusion spontaneously or with treatment.
Binocular vision deficits have been reported to be among the most common vision problems occurring in both the civilian and the military populations after TBI.13,27,39,48-55 Gianutsos27 performed a vision evaluation on a population of 55 severely brain-injured individuals in a rehabilitation facility for individuals requiring long-term treatment. The most common problems found were binocular vision disorders. Cohen et al49 found convergence insufficiency in 38% of acute TBI patients and in 42% of patients reevaluated 3 years after TBI. Suchoff et al48 examined 62 brain-injured patients who resided in extended care facilities and found a high occurrence of exodeviations (41.9%), including convergence insufficiency and intermittent and constant exotropia. There were also a number of patients with vertical deviations (9.7%). Ciuffreda et al39 did a retrospective review of 220 patient records with either TBI or CVA. Vergence deficits (56.3%) were most common in the TBI subgroup, whereas strabismus (36.7%) and cranial nerve palsy (10%) were most common in the CVA subgroup. Convergence insufficiency was the most common dysfunction found in both groups, occurring in 42.5% and 35% of the TBI and CVA patients, respectively.
Studies50,51,52,54,55 conducted among military personnel returning from the wars in Iraq and Afghanistan found a similar pattern after TBI. In these studies, convergence insufficiency was found to be the most common visual disorder after TBI, with a prevalence ranging from 23% to 42%.
In the only study of concussion in the pediatric population, Master et al13 performed a cross-sectional study of the prevalence of vision problems in patients aged 11 to 17 years with a medical diagnosis of concussion. They recruited 100 adolescents with a mean age of 14.5 years. Overall, 69% had one or more vision diagnoses.
ACCOMMODATIVE DISORDERS
The pre-presbyopic, civilian, ABI population consists primarily of TBI. Among this population accommodative disorders, such as accommodative insufficiency, accommodative excess, and accommodative infacility, are more common than among the general clinical population.56,57 Al-Qurainy57 reported that approximately 20% of people with TBI have an accommodative dysfunction. Suchoff et al,48 in a study of 62 consecutive patients with TBI, found that about 10% had accommodative problems. Kowal58 found that 36% of 161 head-injured patients had accommodative problems. In the Ciuffreda et al39 study of 220 patient records with either TBI or CVA, accommodative dysfunction was found (41.1%) in patients with TBI, nearly all of them showing accommodative insufficiency. In contrast, only 12.5% of the patients with CVA had an accommodative disorder. Accommodative problems have also been reported in several case studies.21,32,59,60
In recent studies of military personnel with TBI by Goodrich et al,54 Brahm et al,52 Stelmack et al,50 and Magone et al,55 accommodative dysfunction was found in 22%, 42%, 47%, and 23% of the subjects, respectively. In a study of pediatric patients with concussion, Masters et al found 51% had accommodative dysfunction.13
EYE MOVEMENT DISORDERS
The ocular motor problems present after ABI are different from the developmental eye movement disorders found in the pediatric population (Chapter 22). Saccadic and pursuit anomalies can be caused by abnormalities in the supranuclear control centers for these two functions and their connections to the extraocular muscles. The saccadic and pursuit systems have separate and distinct neurologic pathways (Chapter 13). Because the pathways are separate for saccades and pursuits, ABI can affect one system, leaving the other intact. Thus, if a patient has abnormal pursuit movements with normal saccadic function, a problem in the occipitoparietal supranuclear center should be suspected. Conversely, an abnormality is likely in the frontal eye fields if pursuits are normal but saccades are abnormal. The various types of saccadic and pursuit dysfunction that occur after ABI are summarized in Chapter 13 (Tables 13.2 and 13.3).
In our experience, eye movement disorders are rarely present in isolation after ABI; rather, they are generally found associated with accommodative, binocular, and visual perceptual dysfunctions. As a result, treatment of eye movement deficiencies generally occurs within the context of an overall treatment approach designed to deal with other problems as well.
In a study of pediatric patients with concussion, Masters et al found 29% had saccadic dysfunction based on the results of testing using the Developmental Eye Movement (DEM) Test.13 Suchoff et al48 found that about 40% of ABI patients had eye movement disorders. In a study of civilian population with ABI, Ciuffreda et al39 found deficits of saccades in 51% of patients after TBI and 57% of patients after stroke. The three recent studies of vision disorders in military personnel after TBI revealed a high prevalence of pursuit and saccadic dysfunction, ranging from 6% to 33%.50,52,54 Scheiman and Gallaway32 reviewed treatment results for nine patients after ABI. Two of the nine cases presented had saccadic and pursuit dysfunction. Both of these patients also had binocular vision and accommodative disorders. One of the two cases reported by Cohen38 had eye movement problems, in addition to an exotropia and hypertropia. Ciuffreda et al30 argued that although gross abnormalities in saccadic and pursuit function can be diagnosed using conventional testing and observation, more sophisticated testing may be necessary for patients after ABI. They suggested that, after ABI, it is important to use objective recordings
based on noninvasive infrared technology. The Visagraph (Chapter 1) is an example of the instrumentation that can be used for this purpose. Suchoff et al48 reported on a number of common objectively determined ocular motor deficits associated with CVA; examples include saccadic overshooting and undershooting, difficulty in shifting attention, and inability to sustain fixation and maintain attention.
based on noninvasive infrared technology. The Visagraph (Chapter 1) is an example of the instrumentation that can be used for this purpose. Suchoff et al48 reported on a number of common objectively determined ocular motor deficits associated with CVA; examples include saccadic overshooting and undershooting, difficulty in shifting attention, and inability to sustain fixation and maintain attention.
Symptoms of the Vision Problems Associated with ABI
Most of the symptoms are typical of those experienced by any patient with binocular vision, accommodative, or eye movement disorders and are often associated with reading or other close work (Table 21.1). Common complaints include eyestrain and headaches after short periods of reading, blurred vision, diplopia, loss of place, sleepiness, and difficulty concentrating on reading tasks. In addition, there are some symptoms that are primarily characteristic of patients after ABI. These include poor balance and coordination,21,30,31,61 dizziness,21,31 and light sensitivity.21,31 It is not unusual for patients to report similar symptoms related to distance vision tasks, such as watching television, driving, walking, and sports, particularly in the presence of binocular vision problems such as vertical heterophoria, divergence insufficiency, and cyclophoria. Eye movement and accommodative disorders can also cause symptoms related to distance vision, such as blurred vision, variable vision, and difficulty localizing objects in space.
Evaluation
The customary battery of tests for general binocular vision evaluation, described in Chapter 1 and summarized in Table 21.2, provides the majority of information required for this population. Tests that stress the dynamics of the fusional vergence and accommodative systems and ability to perform well over time are particularly important after ABI. In regard to eye movement testing, Ciuffreda et al29 have stressed the importance of using both chair-side subjective tests (the Northeastern State University College of Optometry Oculomotor Test and DEM Test) and objective eye movement recordings to assess eye movement skills. In our experience, subtle problems can be overlooked unless tests that probe the ability to sustain performance over time and to perform quickly are used. Because cyclovertical heterophoria is common, diagnostic techniques such as the double Maddox rod test (Chapter 14) to detect image tilt are also important. Fixation disparity testing is helpful when dealing with more subtle binocular vision problems and provides valuable information for determining the appropriate prism prescription when necessary. When a patient is symptomatic yet all other testing is negative, it is always important to prescribe diagnostic occlusion (Chapter 14).
In the past decade, researchers and healthcare providers working with patients with concussion have reported the importance of screening/testing for oculomotor disorders as part of the routine concussion workup.19,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76 Mucha et al70 developed a clinical screening test named the Vestibular/Ocular Motor Screening (VOMS) assessment to assess vision and the vestibular system. The test was designed for use by non-eye care professionals to evaluate smooth pursuit, horizontal and vertical saccades, near point of convergence (NPC), horizontal vestibular ocular reflex, and visual motion sensitivity. The testing involves administration of the test and that is followed by the examiner asking the patient how symptomatic they feel after completing the test. They recommended use of the VOMS as a brief vestibular/ocular motor screen after sport-related concussions. Kontos et al77 examined the internal consistency
of the VOMS in a sample of 263 healthy, nonconcussed collegiate athletes. They found that the VOMS possesses internal consistency and an acceptable false-positive rate among healthy Division I collegiate student athletes.
of the VOMS in a sample of 263 healthy, nonconcussed collegiate athletes. They found that the VOMS possesses internal consistency and an acceptable false-positive rate among healthy Division I collegiate student athletes.