• Users Online: 142
  • Print this page
  • Email this page


 
 
Table of Contents
REVIEW ARTICLE
Year : 2021  |  Volume : 3  |  Issue : 1  |  Page : 7

Vision loss and psychopathology


1 UC Davis School of Medicine, University of California, Davis, Sacramento, California, USA
2 Department of Psychiatry and Behavioral Sciences, University of California, Davis, Sacramento, California, USA
3 Department of Ophthalmology and Vision Science, University of California, Davis, Sacramento, California, USA

Date of Submission16-Nov-2020
Date of Acceptance16-Nov-2020
Date of Web Publication10-Feb-2021

Correspondence Address:
Dr. Mark J Mannis
FACS, UC David Health - Eye Center 4860 Y St suite 2400, Sacramento, CA 97817
USA
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/pajo.pajo_65_20

Rights and Permissions
  Abstract 


Purpose: By examining associations between vision loss and various types of psychopathology within the literature, this manuscript will provide ophthalmologists, psychiatrists, and psychologists insight into the relationships between vision and psychopathology to foster cross-professional relations.
Design: Retrospective narrative literature review.
Methods: A narrative literature review was conducted using PubMed, Google Scholar, and Scopus searches. Study types included reviews, case studies, survey analyses, population-based studies, and twin studies, among others. Topics explored include mental health consequences of vision loss, functional neurological disorders and deception syndromes, eye specific personality changes, Charles Bonnet syndrome, and vision disorders associated with psychosis.
Results: Visual impairment correlates with depression and worsened overall quality of life and mental health. Visual health clinicians should improve competencies in basic suicide risk assessments in collaboration with primary care providers and mental health colleagues. When patients with functional neurological disorders or deception syndromes present, understanding their symptoms and motivations is crucial for proper management. Patients with myopia and keratoconus are anecdotally alleged to have unique personalities; however, research shows openness is the only trait correlated with myopia, while a proposed “keratoconus personality” is unfounded. The unique vivid hallucinations of Charles Bonnet syndrome typically do not bother patients and physician reassurance is usually enough to ease the anxious patient. Finally, Usher syndrome involves congenital deafness and progressive blindness in young children with links to psychosis and schizophrenia.
Conclusions: The bidirectional psychosomatic ophthalmological landscape highlights a need to improve screening, recognition, and integrated treatment coordination between visual health providers and mental health providers.

Keywords: Blindness, charles bonnet syndrome, mental health, ophthalmologists, ophthalmology, personality, psychiatry, psychopathology, psychosomatic medicine, psychotic disorders, vision disorders, vision low


How to cite this article:
Mark JR, Kulinich AG, Scher LM, Mannis MJ. Vision loss and psychopathology. Pan Am J Ophthalmol 2021;3:7

How to cite this URL:
Mark JR, Kulinich AG, Scher LM, Mannis MJ. Vision loss and psychopathology. Pan Am J Ophthalmol [serial online] 2021 [cited 2023 Sep 27];3:7. Available from: https://www.thepajo.org/text.asp?2021/3/1/7/309089




  Introduction Top


Ophthalmologists often provide psychological support when a patient is faced with vision loss or a poor prognosis. Furthermore, because of the intimate relationship between vision, our perception of the world, and our ability to navigate the environment, ophthalmologists may be the first person to whom a patient with vision-related psychopathology presents. An important and complex relationship exists between ophthalmologic and psychiatric symptoms, and there is significant literature on the interplay between the two fields. We explore the relationship between vision loss and psychopathology with a review of the existing literature. The topics that we chose to explore include vision loss and its mental health consequences, functional neurological disorders and deception syndromes, personality types associated with specific eye diseases, Charles Bonnet syndrome (CBS), and vision disorders associated with psychosis. By examining the associations between vision loss and various types of psychopathology, this manuscript will provide ophthalmologists, psychiatrists, and psychologists insight into the bidirectional relationships between vision and psychopathology to foster cross-professional insights and more effective professional relationships.


  Visual Impairment and Mental Health Top


Eye disease and vision impairment, whether its onset be sudden or gradual, can be life-changing for an individual. Regardless of the speed, manner, or trajectory of the vision loss, each patient must adjust to sensory change and its consequences. From subtle vision impairment to radical blindness, losing one's sight threatens the potential loss of independence, isolation, or loss of a sense of purpose and motivation. The challenges of navigating daily errands with increased difficulty, reading medication labels, or the inability to perceive facial expressions can be among the significant costs of eye disease. Such vision-associated life changes are emotionally taxing, and it is reasonable to consider related psychopathology and emotional distress in many patients. In this section, we review the impact that vision loss and eye disease have on the mental health of an individual, and we review the prevalence of depression and anxiety.

Exploring the range of ophthalmic pathology and its effect on mental health reveals that there is significant negative impact on mental health across the spectrum of eye disease and vision loss.[1] Quantifying the prevalence and psychological impact of different eye diseases may prove valuable for treatment by offering insight into which patient population carries the highest risk of psychological comorbidity. Due to the high prevalence in the United States, we first consider age-related macular degeneration (AMD) and glaucoma and their associations with patient mental health before considering visual impairment in general.[2],[3],[4],[5]

Age-related macular degeneration

When comparing age-related eye diseases resulting in visual impairment, AMD is the most strongly associated with depressive symptoms.[6],[7] AMD causes moderate-to-severe visual impairment in 8.4 million people across the globe[8] and is responsible for 5%–9% of worldwide blindness.[9],[10] Dawson et al. cross-examined 16 publications to explore the prevalence of depression and anxiety among patients with AMD. Each of the 16 studies found significant prevalence of depressive symptoms 15.7%–44% in patients with AMD when compared to a matched control group.[11] However, the prevalence of anxiety was not consistent with cross-sectional and cohort studies finding AMD and the prevalence of anxiety to be 9.6%–30.1%, while all 7 case–control studies found no significant relationship between anxiety and AMD when compared to control.[11]

Understandably, AMD has dramatic negative effect on the quality of life and life satisfaction among older adults.[12],[13],[14],[15] Brown et al.[14] found significantly reduced quality of life among patients with varying severity of AMD. From mild to very severe AMD, patients suffer a decrease in quality of life from 17% to 60%.[14] Interestingly, Brown et al. also discovered that ophthalmologists substantially underestimated the impact that AMD had on the quality of life of their patients.[14],[15] By recognizing the substantial misjudgment of the impact on quality of life and noting the significant association with worsened mental health outcomes, ophthalmologists can improve care for this disease that is ranked as the third highest cause of severe visual impairment in the world[8] and one that is expected to increase significantly in the rapidly aging U.S.[2],[16]

Glaucoma

Glaucoma is another very common, age-related eye disease that can cause irreparable vision loss and render activities of daily living more difficult.[5],[17],[18] Glaucoma is the fourth-leading cause of moderate-to-severe visual impairment and is responsible for 2.9 million cases of blindness worldwide.[8]

Multiple studies have explored the association between glaucoma and mental health with differing results. Rezapour et al. found no association[19] between self-reported glaucoma and either depression or anxiety among a population-based European cohort. In addition, Jonas et al. and the Beijing Eye Study failed to find any type of glaucoma significantly associated with depression[20] among rural and urban Beijing citizens. Pelčić et al. performed a mini review on the subject and found, of the papers reviewed, that three studies demonstrated no significant prevalence of depression in glaucoma patients,[21] while six studies did find a significant association.[21] Additional studies that found a significant association between glaucoma and depression include the work by Wang et al. that demonstrated a depression prevalence of 10.9% among glaucoma patients with an odds ratio of 1.80,[22] and a study by Popescu et al., which measured a prevalence of 29%.[6] The degree of conflicting measurements warrants future research into the association between mental health and glaucoma, but despite the resulting inconclusiveness, the question's utility should remind the ophthalmologist to consider the possible relationship and have a conversation about fear of vision loss when determining a treatment plan for a patient with glaucoma.

Depression, quality of life, and suicide

The prevalence and magnitude of mental health comorbidities appear to depend on eye pathology among other factors. However, visual impairment in general correlates with depression and a decline in overall quality of life and mental health.[23],[24],[25] The association between visual impairment and mental health comorbidities including stress, depression, anxiety disorders, fear, and social isolation is evident in the literature. Visual impairment contributes to a notable decrease in the quality of life that is seen among patients with vision loss.[25],[26],[27],[28] As such, decreases in quality of life and poor health secondary to visual impairment may contribute to an increase in suicide rates among these patients.[29],[30]

A substantial body of research demonstrates a significant association between depression and visual impairment.[23],[24],[25],[26],[31],[32],[33],[34],[35],[36] A recent, large, longitudinal study conducted in Korea by Choi et al. followed patients with visual impairment who had not previously been diagnosed with depression and found that visual impairment significantly increased the risk of depression over time with a hazard ratio of 1.15 and 1.31 for the nonblindness and blindness groups, respectively.[26]

Visual impairment is not exclusive to older adults and may also negatively affect the mental health of young and working-age adults as well.[36],[37] A cross-sectional study by Zhang et al. measured the prevalence of depression in patients 20 years and older with functional vision loss and found that depression was more than twice as likely among these patients (11.3%) than their counterparts without visual function loss (4.8%).[33] A longitudinal study of adults 65 years and older by Frank et al. showed that the prevalence of clinical symptoms of depression and anxiety were more than twice as likely in patients with self-reported visual impairment than in patients who did not report any visual impairment.[34] The prevalence of depression and anxiety symptoms were 31.2% and 27.2%, respectively, in patients who reported visual impairment, compared to 12.9% and 11.1% of those who did not report visual impairment.[34] Both papers found a significant relationship between self-reported vision loss and depression, and interestingly, both Zhang et al. and Frank et al. found that the reverse was also true. Patients with depressive symptoms were more likely to report visual symptoms.[33],[34] This bidirectional relationship is echoed in other studies where poor vision demonstrably leads to depressive symptoms, and the depressive symptoms lead to worse functional vision.[35] Interestingly, both Zhang et al. and Frank et al. utilized self-reported visual measurements for their comparisons rather than measuring visual acuity.[33],[34] Although visual acuity was not measured in these studies, the relationships they highlighted are germane to delivery of care, since patients' functional vision may be arguably more impactful on quality of life than their objective visual function.[38],[39]

Case report: Suicidal depression in the ophthalmology clinic

Although the relationship and impact of visual impairment on mental health is recurrent in the literature, ophthalmologists commonly underestimate and underrecognize the psychological impact of disease, which can result in delays in appropriate care and referrals to mental health providers.[15],[40],[41] Johnson et al. presented a case study of an older female with monocular blindness secondary to AMD. In this clinical scenario, the patient verbally shared her suicidal thoughts and intent to her visual health providers, including her suicidal plan.[30] After her evaluation from the ophthalmologist, the patient left without further questions or even a basic suicide risk assessment. The ophthalmology resident who interacted with the woman during her visit reached out to the patient several hours later and engaged her primary care physician to assist with safety planning. In this scenario, a crisis was avoided, but this case underlines the importance of gauging the patient response to vision loss and the need for health-care providers to recognize and address statements of depressive symptoms and suicidal intentions infallibly.

Mental health and the ophthalmologist's role

Rees et al. found that only 19% of visually impaired patients with depressive symptoms reported having received any mental health treatment for depression.[40] Furthermore, in a study on mental well-being and the effects of visual impairment by Garcia et al., just over half (52.4%) of patients stated that their source of emotional support was derived from visits with their ophthalmologists.[37] Most patients rely on the ophthalmologists for their psychological support relative to vision loss, yet doctors commonly underestimate the burden of mental health conditions, and only some patients have their depression treated by professionals. With an aging population in the United States, ophthalmology clinics should take steps to improve screening and recognition of common mental health conditions.

Furthermore, as demonstrated in the “near-miss” case report above, visual health clinicians should also improve competencies in basic suicide risk assessments in collaboration with primary care providers and mental health colleagues. It has been shown that approximately 50% of patients who complete suicide have visited a medical professional in the month prior to their death.[42] Nearly half of those that died had opportunities for recognition and possible prevention. Ophthalmologists share the responsibility with all health professionals to implement the basics of suicide prevention. There are available resources, for example, the Suicide Assessment Five-step Evaluation and Triage (SAFE-T) tool, which is supported by the APA and SAMHSA and has been shown to increase inquiry and risk assessment by health-care providers.[43] With resources such as these readily available and with an acknowledgement of responsibility, visual health clinicians can improve the care of their patients' mental health needs.


  Functional Neurological Disorders and Deception Syndromes Top


The eyes serve as the conduit by which the brain processes visual information about its surroundings, but the brain is truly where we see. Just as ocular disease can lead to poor mental health outcomes, so can the mind produce a variety of visual complaints. Functional neurological symptom disorder (FNSD) and factitious disorder (FD) represent two psychiatric diagnoses which intersect with ophthalmology. In this section, we also include a brief discussion on the malingering patient as a related situation which practicing ophthalmologists will encounter.

Functional neurological symptom disorder

FNSD, also known as conversion disorder, is a psychological condition that involves loss of motor or sensory function that cannot be explained by other neurologic or medical findings and may or may not follow a stressful life event.[44] Patients may present with decreased visual acuity or decreased visual field, yet the ophthalmological examination is without abnormal findings that explain the deficit. The neuro-ophthalmological symptoms are termed functional visual loss (FVL) and are considered an unconscious phenomenon that is responsible for approximately 5% of ophthalmology cases and is a common reason for a neurology referral.[44],[45],[46] FVL is more common among women, young adults, and adolescents.[47]

Functional neurological symptom disorder – Case report

Foutch presented a case of a 36-year-old female complaining of a “suddenly blind right eye” following a car accident.[46] At initial visual acuity testing, the patient reported 20/400 OD, 20/25+ OS; the vision improved to 20/50 in the right eye with a pinhole. The woman's visual field testing the following day revealed a completely absent visual field in the right eye and a nasal hemianopia in the left visual field. Foutch then ran the patient through multiple tests to test for visual function, including prism dissociation testing that ultimately confirmed intact vision in the right eye, but abnormal left eye vision. Before referring the patient to neurology, Foutch assessed for life stressors and precipitating factors that may have occurred before the car accident. The patient indicated that a recent death in the family in addition to having her husband's military deployment had left her caring for a young child at home alone. With reassurance, the patient's visual acuity measured 20/20 in both eyes within a matter of minutes. Foutch described the interaction by saying “She cried for 20 min and was 20/20.”Although the typical course of FNSD symptoms is short, usually days, in duration, it should be noted that the above case is atypical in its seemingly instantaneous resolution.[48]

Factitious disorder

FD, previously called Munchausen syndrome, also involves an unconscious motivation. However, these patients consciously create their presenting symptoms for some internal gain, usually related to gains from a “sick role.”[49] Patients may cause physical harm to themselves or present with false or inaccurate histories. The inherent deceitful nature of this condition often makes it difficult to diagnose. The precise prevalence is unknown, but ocular FD is considered relatively uncommon.[50] Similar to FNSD, FD is more commonly observed among women.[49]

Factitious disorder – Case report

Al Ghadeer et al. presented a case of an 18-year-old female with no previous medical history who presented to an ophthalmology emergency department with red, painful eyes and reported seeing ants crawling out of her eyes.[50] After a complete eye examination, the physicians determined that there were no ocular abnormalities. The woman presented the doctors with a cluster of ants that she reportedly had removed from the lower conjunctival fornix, which the lab subsequently confirmed was dead insect particulate matter. The physicians discussed the negative examination findings and recommended a psychiatric evaluation and counseling for the patient yet the patient refuses. The patient and her family promptly left without further treatment. The authors advise ophthalmologists to be vigilant in identifying these patients and following them for continued support, since they commonly return with the same complaint and give no credence to the suggestion that the problem is psychological. In some cases, the patients may visit multiple facilities with the same complaint and receive multiple clinical workups, increasing their risk of iatrogenic illness.

Treatment

In both FNSD and FD, the diagnosis is one of the exclusions. The ophthalmologist must run the patient through a complete eye examination in addition to a battery of additional measures to determine the legitimacy of the patient's complaints. This exclusionary process can consume resources and result in considerable expense for the patient and the facility. Moreover, if the diagnosis of FNSD or FD is made, it is important that the physician avoid passing judgment. The patient's motivation is unconscious, and they have real symptoms even if they are not based in a shared reality. To prevent “therapeutic nihilism” toward such patients, treatment team meetings are recommended to help avoid negative attitudes that may undermine patient care and to help minimize iatrogenic illness.[48] Several different techniques in the management of FD have been described, but there is insufficient clinical evidence that favors one technique as more effective over another.[51] It is advised that the physicians explain the diagnosis to the patient and use medical findings as evidence to discuss the inconsistencies upon completion of the examination.[45],[50] With time, support, and reassurance that no pathological evidence was found on examination, many patients recover completely.[45]

Malingering

Malingering involves a feigned ailment for external personal gain, and unlike FNSD and FD, malingering is consciously motivated. However, similar to the conditions listed above, malingering can also have roots in psychopathology.[52] The reasons for consciously simulating visual disability can be monetarily motivated, occupationally motivated, or for some other external personal gain.[46],[53],[54] These patients typically have poor compliance with testing or treatment, and their symptoms usually disappear when they have acquired what they wished to gain.[52] As with FNSD and FD, this diagnosis is one of the exclusions, and it is important that the ophthalmologist be aware of this possibility when dealing with patients whose complaints do not seem to be explained by the examination. With awareness of the desire for secondary gain, additional unnecessary time and resources can be spared.


  Ocular Disease and Personality Differences Top


Personality is defined as the system of enduring characteristics that contribute to consistency in an individual's thoughts, feelings, and behavior. It is widely accepted that personality is influenced by genetic and environmental factors. The purpose of this section is to investigate the relationship between personality differences and specific ocular conditions. The personalities of patients with myopia and keratoconus are explored as the literature provides many articles on these two demographics. Individuals who are short-sighted (myopic) and patients with keratoconus are anecdotally perceived as having distinctive personality characteristics – introversion in the case of myopia and unusual personality characteristics in keratoconus.[55]

Myopia

The literature is inconclusive with respect to links between personality and myopia.

Numerous studies report that myopic persons tend to be more introverted, tolerant of anxiety, and overcontrolled (low risk taking) than emmetropic persons, but also more self-confident and reflective than persons with hypermetropia.[56],[57],[58]

In contrast to these findings, other studies have suggested that there are no differences in personality characteristics such as extroversion, neuroticism, and social desirability between myopic, hypermetropic, and emmetropic persons.[59],[60],[61],[62] Rodríguez Uña et al. reported a low correlation between myopia and personality and no difference in the degree of myopia between the groups with different education levels. Nonetheless, subjects with more severe ocular pathology associated with myopia had higher scores in neuroticism, without any significant association.[63] Similarly, Van den Berg et al. reported the lack of consistent and meaningful links between personality and myopia in an Australian twin multivariate study using a self-report test and also concluded that myopic persons may reflect intelligence-related stereotypes rather than real correlations with a personality type.

Keratoconus

The literature is similarly inconclusive with respect to associations between personality and keratoconus, and because of this, the relationship between keratoconus and a unique personality has not been established. Numerous studies and reviews report persons with keratoconus described as having an abnormal persona, anxiety, imaginative intuition, and as being more pessimistic, unusual, paranoid, bizarre, demanding, and untrusting.[64],[65] Karseras and Ruben analyzed personality characteristics among patients with keratoconus in 1976. They administered a personality inventory questionnaire to 75 patients with keratoconus and 213 randomly selected patients. This study found no differences between the groups. However, the study limitations in distinguishing the control patients with and without chronic eye disease may have overlooked the impact of chronic eye disease on personality.[66] A study performed years later by Besançon et al. found a larger incidence of “neurological and psychosomatic traits” in patients with keratoconus, but this study was also limited by the lack of a control group.[67]

The first true case–control study among patients with keratoconus was conducted in 1987 by Mannis et al.[68] In this study, the authors utilized the Millon Clinical Multiaxial Inventory to compare the personality traits between patients with keratoconus, patients with chronic eye diseases, and patients without eye disease. They found that patients with keratoconus differed from control patients without eye disease in being less conforming, having more disorganized thoughts, being more passive–aggressive, paranoid, and hypomanic.[68] Patients with chronic eye diseases were found to have similar differences with normal controls, with the addition of being more avoidant, more dependent, and having more borderline personality traits than patients with keratoconus.[68] Years later, Cooke et al. utilized the same methodology as Mannis et al. to compare personality traits of patients with keratoconus to a control group of patients with bilateral myopia of at least 6 diopters.[69] Utilizing the Eysenck Personality Questionnaire and the Maudsley Obsessive–Compulsive Inventory, the authors found no differences in personality or obsessiveness between patients with keratoconus and patient with myopia.[69] The results from Cooke et al. agree with the previous study of Mannis et al., both suggesting that there is no significant difference in personalities between keratoconus and chronic eye disease. Moreover, it can be concluded that a distinct “keratoconus personality” was not found in either study.

In contrast to the studies of Mannis and Cooke, Giedd et al. compared the interactions of keratoconus patients with health-care professionals utilizing the Millon Behavioral Health Inventory database against normal controls and concluded that patients with keratoconus may show less respect and cooperation with health-care providers, which may account for the negative impression of keratoconus patients in the literature.[64] The responses of keratoconus patients were comparable to the responses of patient with chronic eye diseases. This may indicate a relationship between the stress caused by keratoconus as a chronic eye disease. A more recent study by Mannis et al. suggested that the stage of life at which the onset of keratoconus occurs influences the development of personality and coping mechanisms, affecting behavioral patterns and relationships with health-care professionals.[65]

Among the case reports of keratoconus patients, Rudisch et al. presented one case of a 23-year-old male with schizophrenia and a many month history of delusions.[70] The man believed that his corneal transplants, received at the age of 21 years, were radio transmitters. He had been diagnosed with keratoconus at the age of 17 years and had one previous psychiatric hospitalization after a manic episode. He also had a history of polysubstance use disorder. It remains unclear if there was an association between schizophrenia and keratoconus.[70] This relationship requires further investigation.

Based on the aforementioned studies, the relationship between keratoconus and a unique personality cannot be established. However, there appears to be an association between patients with chronic eye disease such as keratoconus, myopia, and others with certain personality traits.[64],[65],[68] In conclusion, patients with keratoconus and other chronic eye diseases may benefit from developing coping mechanisms during the progression of their disease. Consequently, an integrated approach between ophthalmologist and other health-care professionals could aid patients in limiting the psychological stress of their progressive condition.


  Charles Bonnet Syndrome Top


Hallucinations are sensory perceptions in the absence of an external stimulus and are a defining characteristic for psychosis. However, visual hallucinations are not always indicative of a primary psychotic disease and can present in the cognitively competent in the absence of mind-altering substances. One visual hallucination phenomenon that occurs in the visually impaired is CBS, in which patients experience vivid cinematic scenes of varying complexity and theme. These moments may be unnerving for patients, but the concern for their own mental health can even be more frightening as they may assume that they are drifting into insanity. CBS was described 260 years ago by Charles Bonnet, whose grandfather was recorded seeing false imagery despite being blinded by severe cataracts.[71]

These hallucinations are not observed in patients who were born blind, but rather only patients who have their vision impaired later in life.[72] Curiously, the diagnostic criteria of CBS vary across the literature, but the most reliably reported features include vision loss and a full or partial patient understanding that the hallucinations are not reality.[73] Patients vary in their descriptions of the subjects of their hallucinations, but many commonalities exist. For example, the CBS hallucinations often do not typically address the patients, and they commonly include deformed faces or animals.[74],[75]

Pathophysiology of Charles Bonnet syndrome

The consensus is not clear on the pathophysiology of CBS, but the current hypotheses center around the idea of deafferentation in connections with the visual cortex caused by visual impairment, leading to spontaneous activity in the cortex creating hallucinations.[72] Studies conducted on CBS patients using fMRI have shown localized activity in the visual cortex corresponding to the content of the hallucinations.[76] This contrasts with the widespread interconnections one would observe in purposefully imagined visual imagery.[76],[77] Most hallucinations in patients with CBS occur unprovoked, but Menon et al. described various environmental triggers that have been recorded as increasing their occurrence.[72]

Prevalence of Charles Bonnet syndrome

The prevalence of CBS ranges widely across the literature. A review by Plummer et al. found a very broad range of 0.4%–63% in the visually impaired, while a large review by Menon et al. found a more conservatively narrow range of 11%–15%.[71],[72] There appears to be more prevalence among older adults, aged 70–90 years.[78] Differences in experimental methods and underreporting by fearful patients make prevalence difficult to accurately measure.[75] In addition to underreporting by patients, when a patient does decide to present to their physicians, the diagnosis is not uncommonly missed.[71] Teunisse et al. found that only 6% of the patients who discussed their hallucinations with the doctor were given a correct diagnosis, and Gordon and Felfeli showed that most family physicians were not familiar with CBS at all.[78],[79] The lack of recognition combined with underreporting and varying diagnostic criteria creates an unsatisfactory environment for patients with visual impairment that puts them at risk for visual hallucinations.

Treatment of Charles Bonnet syndrome

Treatment for CBS is not always necessary since most patients do not find their hallucinations truly disturbing. Still, the first-line treatment options include physician reassurance and understanding, visual acuity correction if possible, and less commonly, pharmaceuticals such as gabapentin and antipsychotics.[72],[78],[80]

Charles Bonnet syndrome case report

Although most patients are not disturbed by their hallucinations, Issa and Yussuf presented a case of an 85-year-old male with bilateral dry macular degeneration experiencing distressing hallucinations.[80] The patient's family brought the man to the psychiatric clinic for evaluation, where he clearly and competently described the intense visions he was having despite his visual loss. The physician taught the patient behavioral techniques and counseled him on the benign nature of his experience. Thankfully for the patient, the psychiatrist was familiar with CBS, and this patient's symptoms were managed without any medications. This clinical case highlights the importance of conversations between physicians and the visually impaired patient regarding the nature of these visual hallucinations and the reassurance that there is not underlying psychopathology.

Further research into the pathophysiology of CBS will hopefully help explain why this occurs in patients with profound vision loss, and additional exposure in the literature may help raise physician awareness about this phenomenon. Increasing public understanding of CBS may also help patients feel more comfortable speaking with their physicians without the fear of institutionalization if they experience hallucinations themselves.


  Visual Disorders and Psychosis Top


Finally, we look at the relationship between psychosis and vision disorders. There are scarce data about the prevalence of psychotic disorders secondary to vision loss. To date, the literature offers limited information, including case reports, observational studies, and a few reviews. The most common association between visual loss and psychiatric disorders is manifested in Usher syndrome (USH).[81],[82],[83],[84],[85],[86],[87],[88]

Usher syndrome

Usher syndrome is a rare but leading genetic cause of blindness and sensorineural hearing loss with a prevalence in the range of 1–4 per 25,000 people.[89],[90],[91],[92] Usher syndrome is characterized by congenital sensorineural hearing loss, vestibular dysfunction, and retinitis pigmentosa (RP).[93] RP is characterized by progressive degeneration and dysfunction of the retina, primarily affecting rod photoreceptor and pigment epithelial function.[90] The age of onset of both RP and vestibular dysfunction in Usher syndrome is variable.[94],[95]

Early symptoms of RP include night blindness and loss of peripheral vision, caused by degeneration of rod photoreceptors. With progression of RP, cone photoreceptors also degenerate.[90] The loss of central (cone mediated) vision eventually results in patients becoming legally or completely blind.[96],[97]

The most common psychotic symptom reported in Usher syndrome is schizophrenia-like psychosis.[81],[82],[83],[84],[85],[86],[87],[88] In addition, some cases reported an assortment of psychiatric symptoms in Usher syndrome patients, including attention deficit hyperactivity disorder, panic attack, anxiety, depression, and obsessive rituals with psychotic manifestation.[87],[91],[93],[94] The age of onset of psychotic symptoms and RP show no correlation. The literature reveals a clear association between Usher syndrome and psychosis. Nonetheless, it is unclear to what degree the risk of psychosis may relate to intellectual disability, progressive sensory impairment, or even the stress to cope with those sensory deficits. It has been suggested that hallucinations in patients with vision loss are a consequence of abnormal release of central processing, as occurring in CBSs.[87],[89],[90] However, the literature illustrates the difficulty in making a clinical diagnosis of psychosis and intellectual disability in patients with Usher syndrome given the sensory deficits. Multiple authors have suggested an integrated approach to support Usher syndrome patients during the progressive sensory loss to aid them with coping mechanisms and to limit the psychological stress and the development of mental disturbances.[81],[82],[83],[84],[85],[86],[87],[88]


  Conclusions Top


The bidirectionality of the association between visual dysfunction and psychopathology is well demonstrated in the literature. Impaired vision may lead to poor mental health outcomes and vice versa. There is a need to improve screening, recognition, and integrated treatment coordination between visual health providers (ophthalmologists) and mental health providers (psychiatrists, psychologists, and clinical social workers). With recognition of the psychosomatic ophthalmological landscape, doctors can form improved and nuanced treatment plans with mental and emotional health considerations starting at the first visit. The literature suggests that comanagement of these patients with an ophthalmologist alongside a psychiatrist or psychologist could more efficiently manage their holistic care. Communication and coordination between the disciplines is paramount for success in managing these patients.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
McCusker S, Koola MM. Association of ophthalmologic disorders and depression in the elderly: A review of the literature. Prim Care Companion CNS Disord 2015;17:1-4.  Back to cited text no. 1
    
2.
Friedman DS, O'Colmain BJ, Muñoz B, Tomany SC, McCarty C, de Jong PT, et al. Prevalence of age-related macular degeneration in the United States. Arch Ophthalmol Chic Ill 1960 2004;122:564-72.  Back to cited text no. 2
    
3.
Klein R, Chou CF, Klein BE, Zhang X, Meuer SM, Saaddine JB. Prevalence of age-related macular degeneration in the US population. Arch Ophthalmol Chic Ill 1960 2011;129:75-80.  Back to cited text no. 3
    
4.
Shaikh Y, Yu F, Coleman AL. Burden of undetected and untreated glaucoma in the United States. Am J Ophthalmol 2014;158:1121-9.e1.  Back to cited text no. 4
    
5.
Gupta P, Zhao D, Guallar E, Ko F, Boland MV, Friedman DS. Prevalence of Glaucoma in the United States: The 2005-2008 national health and nutrition examination survey. Invest Ophthalmol Vis Sci 2016;57:2577-85.  Back to cited text no. 5
    
6.
Popescu ML, Boisjoly H, Schmaltz H, Kergoat MJ, Rousseau J, Moghadaszadeh S, et al. Explaining the relationship between three eye diseases and depressive symptoms in older adults. Invest Ophthalmol Vis Sci 2012;53:2308-13.  Back to cited text no. 6
    
7.
Eramudugolla R, Wood J, Anstey KJ. Co-morbidity of depression and anxiety in common age-related eye diseases: A population-based study of 662 adults. Front Aging Neurosci 2013;5:56.  Back to cited text no. 7
    
8.
Flaxman SR, Bourne RR, Resnikoff S, Ackland P, Braithwaite T, Cicinelli MV, et al. Global causes of blindness and distance vision impairment 1990-2020: A systematic review and meta-analysis. Lancet Glob Health 2017;5:e1221-34.  Back to cited text no. 8
    
9.
Bourne RR, Stevens GA, White RA, Smith JL, Flaxman SR, Price H, et al. Causes of vision loss worldwide, 1990-2010: A systematic analysis. Lancet Glob Health 2013;1:e339-49.  Back to cited text no. 9
    
10.
WHO Global Data on Visual Impairment. WHO. Available from: http://www.who.int/blindness/publications/globaldata/en/. [Last accessed on 2019 Jun 19].  Back to cited text no. 10
    
11.
Dawson SR, Mallen CD, Gouldstone MB, Yarham R, Mansell G. The prevalence of anxiety and depression in people with age-related macular degeneration: A systematic review of observational study data. BMC Ophthalmol 2014;14:78.  Back to cited text no. 11
    
12.
Mitchell J, Bradley C. Quality of life in age-related macular degeneration: A review of the literature. Health Qual Life Outcomes 2006;4:97.  Back to cited text no. 12
    
13.
Hassell JB, Lamoureux EL, Keeffe JE. Impact of age related macular degeneration on quality of life. Br J Ophthalmol 2006;90:593-6.  Back to cited text no. 13
    
14.
Brown GC, Brown MM, Sharma S, Stein JD, Roth Z, Campanella J, et al. The burden of age-related macular degeneration: A value-based medicine analysis. Trans Am Ophthalmol Soc 2005;103:173-84.  Back to cited text no. 14
    
15.
Brown GC, Brown MM. Health care stakeholder perceptions of vision loss. Surv Ophthalmol 2019;64:345-52.  Back to cited text no. 15
    
16.
Wong WL, Su X, Li X, Cheung CM, Klein R, Cheng CY, et al. Global prevalence of age-related macular degeneration and disease burden projection for 2020 and 2040: A systematic review and meta-analysis. Lancet Glob Health 2014;2:e106-16.  Back to cited text no. 16
    
17.
Glaucoma National Eye Institute. Available from: https://nei.nih.gov/glaucoma/. [Last accessed on 2019 Jun 20].  Back to cited text no. 17
    
18.
Kempen GI, Ballemans J, Ranchor AV, van Rens GH, Zijlstra GA. The impact of low vision on activities of daily living, symptoms of depression, feelings of anxiety and social support in community-living older adults seeking vision rehabilitation services. Qual Life Res 2012;21:1405-11.  Back to cited text no. 18
    
19.
Rezapour J, Nickels S, Schuster AK, Michal M, Münzel T, Wild PS, et al. Prevalence of depression and anxiety among participants with glaucoma in a population-based cohort study: The Gutenberg Health Study. BMC Ophthalmol 2018;18:157.  Back to cited text no. 19
    
20.
Jonas JB, Wei WB, Xu L, Rietschel M, Streit F, Wang YX. Self-rated depression and eye diseases: The Beijing Eye study. PLoS One 2018;13:e0202132.  Back to cited text no. 20
    
21.
Pelčić G, Ljubičić R, Barać J, Biuk D, Rogoić V. Glaucoma, depression and quality of life: Multiple comorbidities, multiple assessments and multidisciplinary plan treatment. Psychiatr Danub 2017;29:351-9.  Back to cited text no. 21
    
22.
Wang SY, Singh K, Lin SC. Prevalence and predictors of depression among participants with glaucoma in a nationally representative population sample. Am J Ophthalmol 2012;154:436-44.e2.  Back to cited text no. 22
    
23.
Varma R, Wu J, Chong K, Azen SP, Hays RD; Los Angeles Latino Eye Study Group. Impact of severity and bilaterality of visual impairment on health-related quality of life. Ophthalmology 2006;113:1846-53.  Back to cited text no. 23
    
24.
McKean-Cowdin R, Varma R, Wu J, Hays RD, Azen SP; Los Angeles Latino Eye Study Group. Severity of visual field loss and health-related quality of life. Am J Ophthalmol 2007;143:1013-23.  Back to cited text no. 24
    
25.
Finger RP, Fenwick E, Marella M, Dirani M, Holz FG, Chiang PP, et al. The impact of vision impairment on vision-specific quality of life in Germany. Invest Ophthalmol Vis Sci 2011;52:3613-9.  Back to cited text no. 25
    
26.
Choi HG, Lee MJ, Lee SM. Visual impairment and risk of depression: A longitudinal follow-up study using a national sample cohort. Sci Rep 2018;8:2083.  Back to cited text no. 26
    
27.
Court H, McLean G, Guthrie B, Mercer SW, Smith DJ. Visual impairment is associated with physical and mental comorbidities in older adults: A cross-sectional study. BMC Med 2014;12:181.  Back to cited text no. 27
    
28.
van der Aa HP, Comijs HC, Penninx BW, van Rens GH, van Nispen RM. Major depressive and anxiety disorders in visually impaired older adults. Invest Ophthalmol Vis Sci 2015;56:849-54.  Back to cited text no. 28
    
29.
Lam BL, Christ SL, Lee DJ, Zheng DD, Arheart KL. Reported visual impairment and risk of suicide: The 1986-1996 national health interview surveys. Arch Ophthalmol 2008;126:975-80.  Back to cited text no. 29
    
30.
Johnson T, Rovner B, Haller J. Suicide and visual loss: A case report reflecting the need for recognition and management in ophthalmological settings. Semin Ophthalmol 2014;29:202-4.  Back to cited text no. 30
    
31.
Evans JR, Fletcher AE, Wormald RP. Depression and anxiety in visually impaired older people. Ophthalmology 2007;114:283-8.  Back to cited text no. 31
    
32.
Rovner BW, Ganguli M. Depression and disability associated with impaired vision: The MoVies Project. J Am Geriatr Soc 1998;46:617-9.  Back to cited text no. 32
    
33.
Zhang X, Bullard KM, Cotch MF, Wilson MR, Rovner BW, McGwin G Jr., et al. Association between depression and functional vision loss in persons 20 years of age or older in the United States, NHANES 2005-2008. JAMA Ophthalmol 2013;131:573-81.  Back to cited text no. 33
    
34.
Frank CR, Xiang X, Stagg BC, Ehrlich JR. Longitudinal associations of self-reported vision impairment with symptoms of anxiety and depression among older adults in the United States. JAMA Ophthalmol 2019;137:793-800.  Back to cited text no. 34
    
35.
Sabel BA, Wang J, Cárdenas-Morales L, Faiq M, Heim C. Mental stress as consequence and cause of vision loss: The dawn of psychosomatic ophthalmology for preventive and personalized medicine. EPMA J 2018;9:133-60.  Back to cited text no. 35
    
36.
Nyman SR, Gosney MA, Victor CR. Psychosocial impact of visual impairment in working-age adults. Br J Ophthalmol 2010;94:1427-31.  Back to cited text no. 36
    
37.
Garcia GA, Khoshnevis M, Gale J, Frousiakis SE, Hwang TJ, Poincenot L, et al. Profound vision loss impairs psychological well-being in young and middle-aged individuals. Clin Ophthalmol Auckl NZ 2017;11:417-27.  Back to cited text no. 37
    
38.
Colenbrander A. Aspects of vision loss Visual functions and functional vision. Vis Impair Res 2003;5:115-36.  Back to cited text no. 38
    
39.
Morse AR. Vision function, functional vision, and depression. JAMA Ophthalmol 2013;131:667-8.  Back to cited text no. 39
    
40.
Rees G, Tee HW, Marella M, Fenwick E, Dirani M, Lamoureux EL. Vision-specific distress and depressive symptoms in people with vision impairment. Invest Ophthalmol Vis Sci 2010;51:2891-6.  Back to cited text no. 40
    
41.
Casten RJ, Rovner BW. Update on depression and age-related macular degeneration. Curr Opin Ophthalmol 2013;24:239-43.  Back to cited text no. 41
    
42.
Ahmedani BK, Simon GE, Stewart C, Beck A, Waitzfelder BE, Rossom R, et al. Health care contacts in the year before suicide death. J Gen Intern Med 2014;29:870-7.  Back to cited text no. 42
    
43.
Brodsky BS, Spruch-Feiner A, Stanley B. The zero suicide model: Applying evidence-based suicide prevention practices to clinical care. Front Psychiatry 2018;9:33.  Back to cited text no. 43
    
44.
Fobian AD, Elliott L. A review of functional neurological symptom disorder etiology and the integrated etiological summary model. J Psychiatry Neurosci JPN 2019;44:8-18.  Back to cited text no. 44
    
45.
Bose S, Kupersmith MJ. Neuro-ophthalmologic presentations of functional visual disorders. Neurol Clin 1995;13:321-39.  Back to cited text no. 45
    
46.
Foutch BK. An atypical presentation of visual conversion disorder. J Optom 2015;8:273-5.  Back to cited text no. 46
    
47.
Lim SA, Siatkowski RM, Farris BK. Functional visual loss in adults and children patient characteristics, management, and outcomes. Ophthalmology 2005;112:1821-8.  Back to cited text no. 47
    
48.
Roberts LW. The American Psychiatric Association Publishing Textbook of Psychiatry. Washington: American Psychiatric Pub; 2019.  Back to cited text no. 48
    
49.
Rosenberg PN, Krohel GB, Webb RM, Hepler RS. Ocular Munchausen's syndrome. Ophthalmology 1986;93:1120-3.  Back to cited text no. 49
    
50.
Al Ghadeer H, Al Othaimeen S, Al Amry M. Ocular Munchausen's Syndrome induced by introduction of ant's particles into the conjunctival fornices. Saudi J Ophthalmol 2018;32:353-4.  Back to cited text no. 50
    
51.
Eastwood S, Bisson JI. Management of factitious disorders: A systematic review. Psychother Psychosom 2008;77:209-18.  Back to cited text no. 51
    
52.
Incesu AI. Tests for malingering in ophthalmology. Int J Ophthalmol 2013;6:708-17.  Back to cited text no. 52
    
53.
Broderick KM, Ableman TB, Weber ED, Enzenauer RW, Wain HJ, Wroblewski KJ. Non-organic vision loss in the Afghanistan and Iraq conflicts. Neuroophthalmology 2017;41:175-81.  Back to cited text no. 53
    
54.
Keltner JL, May WN, Johnson CA, Post RB. The California syndrome. Functional visual complaints with potential economic impact. Ophthalmology 1985;92:427-35.  Back to cited text no. 54
    
55.
van de Berg R, Dirani M, Chen CY, Haslam N, Baird PN. Myopia and personality: The genes in myopia (GEM) personality study. Invest Ophthalmol Vis Sci 2008;49:882-6.  Back to cited text no. 55
    
56.
Lanyon RI, Giddings JW. Psychological approaches to myopia: A review. Am J Optom Physiol Opt 1974;51:271-81.  Back to cited text no. 56
    
57.
Beedle SL, Young FA. Values, personality, physical characteristics, and refractive error. Am J Optom Physiol Opt 1976;53:735-9.  Back to cited text no. 57
    
58.
Baldwin WR. A review of statistical studies of relations between myopia and ethnic, behavioral, and physiological characteristics. Am J Optom Physiol Opt 1981;58:516-27.  Back to cited text no. 58
    
59.
Angi M, Rupolo G, de Bertolini C, Bisantis C. Personality, psychophysical stress and myopia progression. A prospective study on 57 university students. Graefes Arch Clin Exp Ophthalmol 1993;231:136-40.  Back to cited text no. 59
    
60.
Gawron VJ. Ocular accommodation, personality, and autonomic balance. Am J Optom Physiol Opt 1983;60:630-9.  Back to cited text no. 60
    
61.
Gawron VJ. Differences among myopes, emmetropes, and hyperopes. Am J Optom Physiol Opt 1981;58:753-60.  Back to cited text no. 61
    
62.
Bullimore MA, Conway R, Nakash A. Myopia in optometry students: Family history, age of onset and personality. Ophthalmic Physiol Opt 1989;9:284-8.  Back to cited text no. 62
    
63.
Rodríguez Uña I, Pérez Bartolomé F, Urriés Ortiz M, Villalobos PA, Vallecilla MB, Cueto FV, et al. Study of the relationship between myopia and personality. Arch Soc Espanola Oftalmol 2015;90:365-72.  Back to cited text no. 63
    
64.
Giedd KK, Mannis MJ, Mitchell GL, Zadnik K. Personality in keratoconus in a sample of patients derived from the internet. Cornea 2005;24:301-7.  Back to cited text no. 64
    
65.
Mannis MJ, Ling JJ, Kyrillos R, Barnett M. Keratoconus and personality A review. Cornea 2018;37:400-4.  Back to cited text no. 65
    
66.
Karseras AG, Ruben M. Aetiology of keratoconus. Br J Ophthalmol 1976;60:522-5.  Back to cited text no. 66
    
67.
Besançon G, Baikoff G, Deneux A, Mauvoisin M, Bergaud F. Preliminary note on the psychological and mental status of patients with keratoconus. Bull Soc Ophtalmol Fr 1980;80:441-3.  Back to cited text no. 67
    
68.
Mannis MJ, Morrison TL, Zadnik K, Holland EJ, Krachmer JH. Personality trends in keratoconus. An analysis. Arch Ophthalmol 1987;105:798-800.  Back to cited text no. 68
    
69.
Cooke CA, Cooper C, Dowds E, Frazer DG, Jackson AJ. Keratoconus, myopia, and personality. Cornea 2003;22:239-42.  Back to cited text no. 69
    
70.
Rudisch B, D'Orio B, Compton MT. Keratoconus and psychosis. Am J Psychiatry 2003;160:1011.  Back to cited text no. 70
    
71.
Plummer C, Kleinitz A, Vroomen P, Watts R. Of Roman chariots and goats in overcoats: The syndrome of Charles Bonnet. J Clin Neurosci 2007;14:709-14.  Back to cited text no. 71
    
72.
Menon GJ, Rahman I, Menon SJ, Dutton GN. Complex visual hallucinations in the visually impaired: The Charles Bonnet syndrome. Surv Ophthalmol 2003;48:58-72.  Back to cited text no. 72
    
73.
Hamedani AG, Pelak VS. The Charles Bonnet syndrome: A systematic review of diagnostic criteria. Curr Treat Options Neurol 2019;21:41.  Back to cited text no. 73
    
74.
Rovner BW. The Charles Bonnet syndrome: A review of recent research. Curr Opin Ophthalmol 2006;17:275-7.  Back to cited text no. 74
    
75.
Khan JC, Shahid H, Thurlby DA, Yates JR, Moore AT. Charles Bonnet syndrome in age-related macular degeneration: The nature and frequency of images in subjects with end-stage disease. Ophthalmic Epidemiol 2008;15:202-8.  Back to cited text no. 75
    
76.
Ffytche DH, Howard RJ, Brammer MJ, David A, Woodruff P, Williams S. The anatomy of conscious vision: An fMRI study of visual hallucinations. Nat Neurosci 1998;1:738-42.  Back to cited text no. 76
    
77.
Schlegel A, Kohler PJ, Fogelson SV, Alexander P, Konuthula D, Tse PU. Network structure and dynamics of the mental workspace. Proc Natl Acad Sci U S A 2013;110:16277-82.  Back to cited text no. 77
    
78.
Teunisse RJ, Cruysberg JR, Hoefnagels WH, Verbeek AL, Zitman FG. Visual hallucinations in psychologically normal people: Charles Bonnet's syndrome. Lancet 1996;347:794-7.  Back to cited text no. 78
    
79.
Gordon KD, Felfeli T. Family physician awareness of Charles Bonnet syndrome. Fam Pract 2018;35:595-8.  Back to cited text no. 79
    
80.
Issa BA, Yussuf AD. Charles Bonnet syndrome, management with simple behavioral technique. J Neurosci Rural Pract 2013;4:63-5.  Back to cited text no. 80
[PUBMED]  [Full text]  
81.
Mangotich M, Misiaszek J. Atypical psychosis in Usher's syndrome. Psychosomatics 1983;24:674-5.  Back to cited text no. 81
    
82.
Hess-Röver J, Crichton J, Byrne K, Holland AJ. Diagnosis and treatment of a severe psychotic illness in a man with dual severe sensory impairments caused by the presence of Usher syndrome. J Intellect Disabil Res JIDR 1999;43:428-34.  Back to cited text no. 82
    
83.
McDonald C, Kenna P, Larkin T. Retinitis pigmentosa and schizophrenia. Eur Psychiatry 1998;13:423-6.  Back to cited text no. 83
    
84.
Waldeck T, Wyszynski B, Medalia A. The relationship between Usher's syndrome and psychosis with Capgras syndrome. Psychiatry 2001;64:248-55.  Back to cited text no. 84
    
85.
Jumaian A, Fergusson K. Psychosis in a patient with Usher syndrome: A case report. East Mediterr Health J 2003;9:215-8.  Back to cited text no. 85
    
86.
Wu CY, Chiu CC. Usher syndrome with psychotic symptoms: Two cases in the same family. Psychiatry Clin Neurosci 2006;60:626-8.  Back to cited text no. 86
    
87.
Rijavec N, Grubic VN. Usher syndrome and psychiatric symptoms: A challenge in psychiatric management. Psychiatr Danub 2009;21:68-71.  Back to cited text no. 87
    
88.
Domanico D, Fragiotta S, Trabucco P, Nebbioso M, Vingolo EM. Genetic analysis for two italian siblings with usher syndrome and schizophrenia. Case Rep Ophthalmol Med 2012;2012:380863.  Back to cited text no. 88
    
89.
Boughman JA, Vernon M, Shaver KA. Usher syndrome: Definition and estimate of prevalence from two high-risk populations. J Chronic Dis 1983;36:595-603.  Back to cited text no. 89
    
90.
Hartong DT, Berson EL, Dryja TP. Retinitis pigmentosa. Lancet 2006;368:1795-809.  Back to cited text no. 90
    
91.
Keats BJ, Corey DP. The usher syndromes. Am J Med Genet 1999;89:158-66.  Back to cited text no. 91
    
92.
Kimberling WJ, Hildebrand MS, Shearer AE, Jensen ML, Halder JA, Trzupek K, et al. Frequency of Usher syndrome in two pediatric populations: Implications for genetic screening of deaf and hard of hearing children. Genet Med 2010;12:512-6.  Back to cited text no. 92
    
93.
Hope CI, Bundey S, Proops D, Fielder AR. Usher syndrome in the city of Birmingham Prevalence and clinical classification. Br J Ophthalmol 1997;81:46-53.  Back to cited text no. 93
    
94.
Keats BJ, Savas S. Genetic heterogeneity in Usher syndrome. Am J Med Genet A 2004;130A: 13-6.  Back to cited text no. 94
    
95.
Tsilou ET, Rubin BI, Caruso RC, Reed GF, Pikus A, Hejtmancik JF, et al. Usher syndrome clinical types I and II: Could ocular symptoms and signs differentiate between the two types? Acta Ophthalmol Scand 2002;80:196-201.  Back to cited text no. 95
    
96.
Edwards A, Fishman GA, Anderson RJ, Grover S, Derlacki DJ. Visual acuity and visual field impairment in Usher syndrome. Arch Ophthalmol 1998;116:165-8.  Back to cited text no. 96
    
97.
Fishman GA, Bozbeyoglu S, Massof RW, Kimberling W. Natural course of visual field loss in patients with Type 2 Usher syndrome. Retina 2007;27:601-8.  Back to cited text no. 97
    




 

Top
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
Abstract
Introduction
Visual Impairmen...
Functional Neuro...
Ocular Disease a...
Charles Bonnet S...
Visual Disorders...
Conclusions
References

 Article Access Statistics
    Viewed4597    
    Printed118    
    Emailed2    
    PDF Downloaded303    
    Comments [Add]    

Recommend this journal