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Anxiety and Charles Bonnet syndrome.

Abstract: Introduction: Some persons with Charles Bonnet syndrome (CBS) suffer significant anxiety because of their visual hallucinations, while others do not. The aim of the study presented here was to compare levels of anxiety in persons with low vision with and without CBS. Methods: This retrospective study compared the level of anxiety in 31 persons with CBS and 26 persons without CBS. These participants were recruited voluntarily from senior centers, a low vision support group, and an ophthalmology practice in October and November 2010. All were administered surveys to measure cognitive function (TICS: Telephone Interview for Cognitive Status), anxiety (STAI: State and Trait Anxiety Inventory), and general health (GHQ: General Health Questionnaire). The responses of the two groups were compared. Results: The participants with CBS exhibited higher levels of anxiety than did those without CBS on both the STAI and GHQ surveys, but this difference did not reach statistical significance. The proportion of participants who were pharmacologically treated for anxiety was four times higher in the CBS cohort than in the cohort without CBS: CBS: 36% (11 of 31), those without CBS: 9% (2 of 22), p value = .03. The participants with CBS who took medication for anxiety scored higher on the STAI and GHQ than did those without CBS, but these differences did not reach statistical significance. Discussion: The findings indicate that persons with CBS have higher levels of anxiety than do those without CBS. The highest levels of anxiety occurred in the participants with CBS who were being treated for anxiety with medications. Although the findings did not reach statistical significance, they suggest that anxiety is an important consideration when treating individuals with CBS. Implications for practitioners: Persons with CBS who have difficulty tolerating visual hallucinations may benefit from interventions that are directed at managing anxiety, such as counseling, visual rehabilitation, and pharmacological treatment.

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Charles Bonnet syndrome (CBS) is characterized by complex visual hallucinations in psychologically normal people with low vision (Shiraishi, Terao, Ibi, Nakamura, & Tawara, 2004) The disorder typically occurs in older adults and in a wide spectrum of ophthalmic diseases, with macular degeneration being the most common. Estimates of the frequency of CBS range from 10% to 30% of persons with low vision (Scott, Schein, Feuer, & Folstein, 2001). Due to the sensitive and potentially embarrassing nature of the hallucinations, many elderly persons do not report their symptoms (Menon, Rahman, Menon, & Dutton, 2003). Anxiety is defined as a neurosis characterized by excessive worry and overconcern. It is frequently associated with somatic symptoms, such as restlessness, sleep disturbance, and difficulty concentrating (Menon et al., 2003). The prevalence of anxiety in older adults aged 55 to 85 years has been estimated at about 10% (Beekman et al., 1998). Treatment may consist of psychotherapy, pharmacotherapy, or both. Medications to control the symptoms of anxiety include benzodiazepines, selective serotonin reuptake inhibiters, serotonin-nor epinephrine reuptake inhibitors, and antipsychotics (Gorman, 2002).

Funding for the research presented in this article was provided by the Center for Eye Research and Education and the Barnstable Yarmouth Lions Clubs and is gratefully acknowledged. We thank Sight Loss Services for its support and dedication throughout this study. This article is dedicated to June Wenberg.

Several studies have been conducted to investigate the epidemiology, possible psychiatric morbidity, and phenomenology of the visual hallucinations in those with CBS. Still, much remains to be understood about the syndrome. Scott et. al. (2001) concluded that visual hallucinations in a population of persons with glaucoma were common; underdiagnosed; and not associated with cognitive deficits, abnormal personality traits, or a family or personal history of psychiatric morbidity. The authors demonstrated that persons with CBS are likely to become distressed and anxious as a result of visual hallucinations that are typical of the disease, particularly when the etiology of the origins of the hallucinations had not been previously explained. Holroyd et al.'s (1992) study on the visual hallucinations of persons with macular degeneration showed that CBS appeared unrelated to the primary psychiatric disorder. We have noted in clinical practice that some persons suffer significant stress and anxiety because of their hallucinations, while others tolerate the experience without much apparent bother. The anguish can occur for a variety of reasons: the intrusive and bothersome nature of the hallucinations, the implications of mental instability, the occasionally frightening or disturbing characteristics of the hallucinations, and the lack of knowledge or understanding of the origins of the phenomenon. The study presented here was designed to measure the levels of anxiety in a population of persons with low vision who had CBS and to compare the results to a population of persons with visual impairments who did not have CBS.

Materials and methods

The study received approval from the Western Institutional Review Board, and informed consent was obtained from all the participants. The participants were recruited from three sources: senior centers (local organizations that provide older persons with a location for socialization and information based in each town); Sight Loss Services, a local nongovernmental, nonprofit organization that is designed to assist persons with low vision; and an outpatient private ophthalmology office at Ophthalmic Consultants of Boston. Notification of the study was posted in fliers and newsletters (font size 28), requesting persons with visual impairments to volunteer to participate in a research study about low vision and visual hallucinations. The fliers and newsletters specifically targeted persons with low vision who had and did not have visual hallucinations. Potential participants were asked to call in on their own or with the assistance of Sight Loss Services and Ophthalmic Consultants of Boston to register for the study. To be part of the study, they were not required to leave their homes.

Legal blindness, with a visual acuity worse than 20/200 in the better eye, was a required criterion for participation in the study. Visual acuity was measured with a Snellen chart, both with spectacle correction and with a pinhole occluder. Visual acuity was not formally obtained for four CBS participants and one non-CBS (N-CBS) participant because for these participants, the testing was done in their homes without a Snellen chart, but all had legal blindness (20/200 or worse). Exclusionary criteria for the participants were persons with migraine-related visual auras, seizures, Parkinson's disease, schizophrenia, posttraumatic stress disorder, and those who scored "mildly impaired" or worse on the Telephone Interview for Cognitive Status. The study was conducted over a period of two months from October 2010 through November 2010.

The participants were divided into two groups: those with CBS and those without CBS (N-CBS) on the basis of the diagnostic criteria for CBS, established in 1996 by Teunisse, Cruysberg, Hoefnagels, Verbeek, and Zitman (1996). These diagnostic criteria included the presence of at least one hallucination within the past four weeks, a period between the first and the previous hallucination exceeding four weeks, full or partial retention of insight into the unreal nature of the hallucinations, the absence of hallucinations in other sensory modalities, and the absence of delusions. Hallucinations were described as complex and visual excluding flashes of light, halos, and other common occurrences in people suffering from other eye diseases, such as glaucoma and retinal detachment. The participants who answered positively to any of these aforementioned criteria were interviewed on the characteristics of the hallucinations to ensure that the hallucinations were of the type that is typically seen in persons with CBS and were referred to in the study.

The participants were considered to be under treatment for anxiety if they answered yes to two questions: "Are you currently being treated for anxiety by your medical doctor?" and "Are you currently taking prescription medication for anxiety?" The medications that were taken included duloxetine, citalopram, paroxetine, lorazepam, and alprazolam. Emphasis was placed on medications that were taken specifically for anxiety. Formal psychiatric testing was not performed.

Three survey tools were used to gather data from the participants. Cognitive function was assessed in all the participants with the Telephone Interview for Cognitive Status (TICS) for the purpose of evaluating for dementia or delirium (Brandt, Spencer, & Folstein, 1988). TICS was selected because of its accessibility for persons who are visually impaired (Scott et al., 2001). It has been shown to correlate highly with the Mini-Mental State examination (Folstein, Folstein, & McHugh, 1975). The General Health Questionnaire (GHQ-12) was used to measure levels of anxiety (Goldberg, 1978). Selected because of its utility as a screening questionnaire for emotional distress, the GHQ's validity has been affirmed in several studies (see, for example, Tennant, 1977). A higher score corresponds to increased anxiousness. The State and Trait Anxiety Inventory (STAI; Spielberger, Gorsuch, Lushene, Vagg, & Jacobs, 1970) was selected as a second tool for measuring anxiety. It was chosen because of its ability to differentiate between the temporary condition of "state anxiety" and the more general and longstanding quality of "trait anxiety." As Spielberger noted,
   Trait Anxiety implies differences between
   people in the disposition to
   respond to stressful situations with
   varying amounts of State Anxiety.
   But whether or not people who differ
   in Trait Anxiety will show corresponding
   differences in S-Anxiety
   depends on the extent to which each
   of them perceives a specific situation
   as psychologically dangerous or
   threatening.


The STAI has 40 questions consisting of two 20-item scales, with a range of four possible responses to each. It has been validated in a number of studies (Gorenstein & Andrade, 1996). The surveys were administered by four of the authors (Anna Geueke, Angeliki Lambrou, Katharine Morley, and Michael G. Morley), as well as by two volunteers who were trained to administer the surveys.

Descriptive statistics were computed for the description of the study population. We evaluated whether the continuous variables followed the normal distribution by graphical inspection (histograms, box plots, and normal probability plots) and by using normality tests (Shapiro Wilk). The Wilcoxon Mann-Whitney two-sample rank-sum test was used to compare two groups of non-normally distributed continuous variables, while the chi-square or Fisher's exact tests were used to test for group differences in the categorical variables. All tests were two tailed. The Bonferonni correction was applied to the results. With 14 total comparisons, our p value for statistical significance for the entire project was 0.05/14 or .004. All statistical analyses were conducted using SAS (version 9.2 SAS Institute, Cary, NC). We certify that all applicable institutional and governmental regulations concerning the ethical use of human volunteers were followed during the research.

Results

The demographic characteristics of the participants are shown in Table 1. The age, sex, visual acuity in the better eye, and percentage with macular degeneration of the 31 participants with CBS and the 26 participants without CBS were similar and not statistically different. The cognitive status in both groups measured "nonimpaired" in both groups, but the CBS group scored higher on cognitive status, a difference that was statistically significant.

As a group, the participants with CBS exhibited higher levels of anxiety than did the N-CBS participants when measured with both the STAI and GHQ surveys (see Table 2), but these differences did not reach statistical significance when the Bonferonni correction was applied. On the STAI survey, both state and trait levels of anxiety were higher in the participants with CBS than in the N-CBS participants. The GHQ results also showed higher levels of anxiety in the CBS participants compared to the N-CBS participants, but not at a level that reached statistical significance. The difference between the state and trait levels of anxiety within the CBS and N-CBS groups was small and not statistically significant.

The proportion of participants who were pharmacologically treated for anxiety in the CBS cohort was four times higher than the proportion in the N-CBS cohort: CBS participants, 36% (11 of 31); N-CBS participants, 9% (2 of 22), p value = .03. The participants with CBS who took medication for anxiety scored higher on the GHQ than did the N-CBS participants (see Table 3). The same was true when anxiety levels were evaluated by both sections of the STAI, but these differences did not reach statistical significance.

In the CBS cohort, the duration of hallucinations ranged from 3 months to 10 years, with a mean duration of 38.2 months. The CBS cohort reported a wide variety in the content of the hallucinations. Examples of content included small people in costume, piles of bricks, green wallpaper, lips, wild horses, and a gruesome pirate's head.

Discussion

Our clinical impression from caring for persons with low vision who have CBS was that some patients struggle considerably while others seem to tolerate their hallucinations without much bother. The results of this study support that impression and confirm the findings of Gilmour, Schreiber, and Ewing (2009), who reported that 36% of their participants self-reported a negative reaction to CBS hallucinations. The STAI and GHQ results corroborate the impression that persons with CBS, on average, suffer from more anxiety than their counterparts without CBS. When broken down by absolute score, there is a wide range of levels of anxiety, with some persons with CBS having relatively little anxiety and some having considerable anxiety. The highest levels of anxiety in the study occurred in the group with CBS who were being treated for anxiety with medications. It is interesting that within the CBS group, the state and trait anxiety measurement results were similar. This finding suggests that persons with CBS do not perceive hallucinations, by themselves, to be the cause for their anxiety (that is, those with CBS are indeed more anxious, but not necessarily because of their hallucinations). In conclusion, our findings support the clinical impression that persons with low vision who have CBS have higher levels of anxiety than do those without CBS. This relationship would benefit from further study.

This retrospective study suffered from several significant weaknesses and sources of potential bias. Recruiting participants with CBS can be difficult, since they are elderly, cannot read or drive, and may have comorbidities of age. The number of participants in the study was small, making comparisons of subgroups difficult. Within the N-CBS group, only 2 participants (9%) were taking anxiety medications, which was expected, given the 10% reported prevalence of anxiety in elderly persons. However, this small number limited our ability to compare precisely the anxiety levels of the CBS and N-CBS participants who were receiving treatment for anxiety. Although no statistically significant differences were detected when we measured anxiety levels using the STAI survey, the 11 CBS participants who were receiving anxiety medications showed much higher anxiety levels than did the 2 N-CBS participants who were also treated for anxiety. Our process of recruiting participants with low vision in physicians' offices, senior centers, and blindness support groups was a potential source of bias. Another weakness of our study was our reliance on the participants' responses regarding the diagnosis of anxiety and a review of their lists of medications. A formal neuropsychiatric evaluation would have been more accurate in establishing the diagnosis of anxiety. We also acknowledge that the measurement of visual impairment by visual acuity alone did not take into account the actual functional status of the participants, which could have affected the development of CBS hallucinations and anxiety.

Although this article points out the association between CBS and anxiety, it does not define the relationship between the anxiety and the hallucinations. There is relatively little information in the literature regarding anxiety and CBS hallucinations. One article suggested that 34% of the participants initially had a self-reported "negative reaction" to CBS hallucinations, but after one year that figure dropped to 18% (Gilmour et al., 2009). However, that article did not answer the question of whether hallucinations lead to anxiety or whether anxiety predisposes a person to hallucinations. It may well be that the relationship is more complex than a simple cause and effect, but the impression that there is a relationship between persons with CBS and anxiety warrants further study on the basis of our clinical observations and the results of this study. The neuropsychiatric literature is beginning to investigate the relationship among cognitive factors, mental states, and hallucinations, but there are no definitive answers to this complex question (Morrison, Wells, & Nothard, 2000).

Relatively few participants described hallucinations that were disturbing because of the content or nature of the hallucinations. Unpleasant insects or terrifying images occurred in the hallucinations of only three participants, but they were deeply disturbing to those who were affected. More commonly, the hallucinations were unwelcome and intrusive rather than disturbing.

The conclusion that persons with CBS have higher levels of anxiety than do persons without CBS has implications for primary care physicians and ophthalmologists who treat persons with CBS, especially at the initial presentation. Many participants indicated that they "got used to" their hallucinations as time went on. This finding suggests that the initial onset of hallucinations is the period of greatest discomfort and aggravation. Most participants seemed to accommodate the hallucinations without excessive anxiety, but nearly one-third of the participants with CBS were under pharmacological treatment for anxiety. Referral for evaluation and treatment of anxiety, including counseling and support groups, visual rehabilitation, and medication (if necessary), may be helpful to persons with CBS. This finding stresses the importance of the thorough education of patients and physicians on CBS. Also, it is paramount that physicians inquire about hallucinations in persons with severe visual impairments to provide reassurance to those who may be experiencing them.

Some of the time-tested approaches to managing CBS include taking time to explain the syndrome and reassuring persons that their cognitive status is entirely normal. Indeed, many of participants with CBS were relieved to hear that CBS is an established disorder that is not related to mental illness. Most reported a decreasing frequency of hallucinations over time and that was reassuring to some participants as well. Jackson and Bassett (2010) reported that 28% of persons with CBS with hallucinations will cease having them after one year, which may comfort some persons.

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References

Beekman, A. T., Bremmer, M. A., Deeg, D. J., van Balkom, A. J., Smit, J. H., de Beurs, E., van Dyck, R., & Tilburg, W. (1998). Anxiety disorders in later life: A report from the longitudinal aging study Amsterdam. International Journal of Geriatric Psychiatry, 13, 717-726.

Brandt, J., Spencer, M., & Folstein, M. (1988). The Telephone Interview for Cognitive Status. Neuropsychiatry, Neuropsychology, & Behavioral Neurology, 1(2), 111-117.

Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). "Mini-mental State": A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189-198.

Gilmour, G., Schreiber, C., & Ewing, C. (2009). An examination of the relationship between low vision and Charles Bonnet syndrome. Canadian Journal of Ophthalmology/Journal Canadien d'Ophtalmologie, 44(1), 49-52.

Goldberg, D. P. (1978). General Health Questionnaire (GHQ). Windsor, England: NFER Publishing.

Gorenstein, C., & Andrade, L. (1996). Validation of a Portuguese version of the Beck Depression Inventory and the State-Trait Anxiety Inventory in Brazilian subjects. Brazilian Journal of Medical and Biological Research, 29, 453-457.

Gorman, J. M. (2002). Treatment of generalized anxiety disorder. Journal of Clinical Psychiatry, 63, Suppl. 8, 17-23.

Holroyd, S., Rabins, P. V., Finkelstein, D., Nicholson, M. C., Chase, G. A., & Wisniewski, S. C. (1992). Visual hallucinations in patients with macular degeneration. American Journal of Psychiatry, 149, 1701-1706.

Jackson, M. L., & Bassett, K. L. (2010). The natural history of the Charles Bonnet syndrome: Do the hallucinations go away? Eye, 24, 1303-1304.

Menon, G. J., Rahman, I., Menon, S. J., & Dutton, G. N. (2003). Complex visual hallucinations in the visually impaired: The Charles Bonnet syndrome. Survey of Ophthalmology, 48, 58-72.

Morrison, A. P., Wells, A., & Nothard, S. (2000). Cognitive factors in predisposition to auditory and visual hallucinations. British Journal of Clinical Psychology, 39, 67-78.

Scott, I. U., Schein, O. D., Feuer, W. J., & Folstein, M. F. (2001). Visual hallucinations in patients with retinal disease. American Journal of Ophthalmology, 131, 590-598.

Shiraishi, Y., Terao, T., Ibi, K., Nakamura, J., & Tawara, A. (2004). The rarity of Charles Bonnet syndrome. Journal of Psychiatric Research, 38, 207-213.

Spielberger, C. D., Gorsuch, R. L., Lushene, R., Vagg, P. R., & Jacobs, G. A. (1970). Manual for the State-Trait Anxiety Inventory. Mountain View, CA: Consulting Psychologists Press.

Tennant, C. (1977). The General Health Questionnaire: A valid index of psychological impairment in Australian populations. Medical Journal of Australia, 2, 392-394.

Teunisse, R. J., Cruysberg, J. R., Hoefnagels, W. H., Verbeek, A. L., & Zitman, F. G. (1996). Visual hallucinations in psychologically normal people: Charles Bonnet's syndrome. Lancet, 347(9004), 794-797.

Anna Geueke, B.A., R.N., registered nurse, Graduate School of Nursing, University of Massachusetts at Worcester, 55 North Lake Avenue, Worcester, MA 01605; e-mail: <anna.geueke@gmail.com>. Michael G. Morley, M.D., M.H.C.M., assistant clinical professor of ophthalmology, Center for Eye Research and Education, 50 Staniford Street, Suite 600, Boston, MA 02114; e-mail: <mgmorley@gmail. com>. Katharine Morley, M.D., M.P.H., clinical instructor in medicine, Harvard Medical School, 23 Kenilworth Street, Newton, MA 02458; e-mail: <katharinemorley@gmail.com>. Alice Lorch, M.D., mailing address: 37 Lee Street, Apartment 3, Cambridge, MA 02139; e-mail: <alice_lorch@ meei.harvard.edu>. MaryLou Jackson, M.D., vision rehabilitation specialist and director, Vision Rehabilitation Center, Massachusetts Eye and Ear Infirmary, 243 Charles Street, Boston, MA 02114; e-mail: <marylou@mljackson.ca>. Angeliki Lambrou, R.N., M.P.H., Sc.D., mailing address: 203 Park Drive, Apartment G-10, Boston, MA 02215; e-mail: <alambrou@hsph.harvard.edu>. June Wenberg, B.A., director of support groups and outreach, Sight Loss Services, P.O. Box 414, 81 School Street, West Dennis, MA 02670; e-mail: <jscully@ jwen.com>. Afua Oteng-Amoako, O.D., M.P.H., doctoral student in public health, Harvard School of Public Health, 677 Huntington Avenue, Boston, MA 02115-6018; e-mail: <afuaamoako@gmail.com>.
Table 1
Demographic characteristics of the samples.

                                Question 1   Question 2
Variable                          sample       sample

Age (at Wave 4)
  19                                5            1
  20                                22           7
  21                                25           33
  22                                32           37
  23                                15           22
Gender
  Male                              56           52
  Female                            44           48
Race or ethnicity
  White                             65           63
  African American                  21           24
  Hispanic                          12           11
  Asian American or Pacific
    Islander                        2            2
Parents report youth is blind       36           31
Youth has a secondary
  disability                        38           28
Attending postsecondary
  school (at Wave 4)                33           36
Working 20 hours or more per
  week (at Wave 4)                  29           43

Note: All figures are reported in percentages
without decimal places, per Institute of Education
Sciences guidelines.

Table 2
Results of the State and Trait Anxiety Inventory (STAI) and the
General Health Questionnaire (GHQ), given as the median
(interquartile) for the participants with and without Charles Bonnet
syndrome (CBS).

                    CBS               Non-CBS
                participants        participants
                                                       p values
STAI and GHQ   N       Median      N       Median        (a)

STAI: State    30   37.0 (24.0)    25   27.0 (13.0)      0.01
STAI: Trait    30   35.5 (16.0)    25   29.0 (12.0)      0.02
GHQ            31    2.0 (5.0)     26    1.0 (3.0)       0.11

(a) p values for differences between patients with and without CBS
from the Wilcoxon-Mann-Whitney two-sample rank-sum test. The
differences were not statistically significant after the Bonferonni
correction was applied.

Table 3
Scores on the State and Trait Anxiety Inventory (STAI) and the General
Health Questionnaire (GHQ), given as the median (interquartile), among
the participants with and without Charles Bonnet syndrome (CBS),
stratified by treatment for anxiety.

                               CBS          Non-CBS      p values
Treatment for anxiety      participants   participants     (a)

Receiving treatment for anxiety
  Number of participants        11             2
  STAI score: State        50.0 (27.0)     22.5(l.0)       0.10
  STAI score: Trait        37.0 (12.0)     28.5(l.0)       0.06
  GHQ score                 4.0 (7.0)      0.5 (1.0)       0.04

Receiving no treatment for anxiety
  Number of participants        19             20
  STAI score: State        30.0 (13.0)    28.5 (14.0)      0.21
  STAI score: Trait        31.0 (19.0)    29.0 (15.0)      0.19
  GHQ score                 1.0 (5.0)      1.0 (3.5)       0.89

(a) p values for differences between the participants with and without
CBS from the Wilcoxon-Mann-Whitney two-sample rank-sum test. The
differences were not statistically significant after the Bonferonni
correction was applied.
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Article Details
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Title Annotation:CEU Article
Author:Geueke, Anna; Morley, Michael G.; Morley, Katharine; Lorch, Alice; Jackson, MaryLou; Lambrou, Angeli
Publication:Journal of Visual Impairment & Blindness
Article Type:Report
Date:Mar 1, 2012
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