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The rarity of Charles Bonnet syndrome
Journal of Psychiatric Research 38 (2004) 207–213 www.elsevier.com/locate/jpsychires
The rarity of Charles Bonnet syndrome Yasuko Shiraishia, Takeshi Teraoa,*, Kenji Ibib, Jun Nakamuraa, Akihiko Tawarab a Department of Psychiatry, University of Occupational and Environmental Health School of Medicine, Kitakyushu, Japan Department of Opthalmology, University of Occupational and Environmental Health School of Medicine, Kitakyushu, Japan
b
Received 11 November 2002; received in revised form 7 May 2003; accepted 11 June 2003
Abstract Charles Bonnet syndrome (CBS) is characterized by complex visual hallucinations in otherwise psychologically normal people. Estimates of the prevalence of CBS in different samples vary from a small percentage (around 1%), to a relatively large percentage (about 10%). The purpose of the present study is to determine whether CBS is rare or not. One-thousand ophthalmologic and optometric outpatients at a university hospital were consecutively screened by a questionnaire to identify patients possibly experiencing visual hallucinations. The mean corrected visual acuity in the best eye was 1.1. Those who positively responded to the questionnaire were further investigated to determine whether their symptoms were consistent with CBS. As a result, the prevalence of CBS was 0.5% (5/1000). In subclass analyses, the prevalence was 3 of 372 (0.8%) in the low vision group, 2 of 346 (0.6%) in the elderly, and 1 of 120 (0.8%) in both conditions. These were not significantly different from each other or from the overall prevalence (0.5%). This low prevalence of CBS in our subjects may be due to their relatively good visual acuity because previous studies with high prevalence of CBS investigated patients with a visual acuity of less than 0.3. The prevalence of CBS may be low in patients with these particular characteristics, and this syndrome seems to be rare in even ophthalmologic and optometric patients if they do not have seriously low vision. Further studies are needed to investigate the prevalence of CBS in general population. # 2003 Elsevier Ltd. All rights reserved. Keywords: Charles Bonnet syndrome; Visual hallucinations; Visual acuity; Advanced age; Prevalence
1. Introduction Charles Bonnet syndrome (CBS) was named after the Swiss Philosopher who first described the occurrence of vivid complex visual hallucinations in his visually impaired, otherwise psychologically normal, grandfather Charles Lullin in 1760 (Damas-Mora et al., 1982). Since then, the disorder has been widely reported but estimates of prevalence vary considerably from study to study from as low as 0.4% (Adachi, 1996) to as high as 12% (Teunisse et al., 1996). As such, it is presently uncertain whether CBS is rare or not. An explanation for differences in the reported prevalence of CBS may lie in the different diagnostic criteria applied and the samples used to investigate the disorder. There have been five sets of diagnostic criteria (Damas-Mora et al., 1982; Teunisse et al., 1996; Gold * Corresponding author. Tel.: +81-93-691-7253; fax: +81-93-6924894. E-mail address: [email protected] (T. Terao). 0022-3956/$ - see front matter # 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0022-3956(03)00090-6
and Rabins, 1989; Podoll et al., 1990; Ball, 1991) for CBS and, with the exception of Ball (1991), all included the presence of insight to visual hallucinations; thus ‘‘psychological normality’’ may be at least partially guaranteed in CBS patients (Terao and Collinson, 2001; Terao, 2002). In addition, the above-mentioned criteria do not require the presence of optic pathology, although clinicians commonly associate CBS with eye diseases (Fernandez et al., 1997). Thus, low visual acuity is not necessary for diagnosing CBS, but there remains a possibility that in some CBS patients low visual acuity may actually bring about visual hallucinations. In any case, these criteria seem to be relatively consistent in diagnosing visual hallucinations in otherwise psychologically normal people but have nevertheless been applied to a range of very different samples from ophthalmologic patients to psychogeriatric patients (Terao, 2002). Another possible reason for differences in the reported prevalence of CBS is that all of the abovementioned diagnostic criteria have been derived almost exclusively from cross-sectional observations. It is therefore
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possible that some patients with dementia manifest complex visual hallucinations in the early stages of the illness and they may be inappropriately diagnosed as suffering from CBS (Terao & Collinson, 2000; Pliskin et al., 1996). Conversely, it is also possible that visual hallucinations in patients with dementia may be not only due to dementia itself, but also due to CBS (Terao, 2000a,b). Recently, Terao (2002) reviewed the pertinent references to CBS, and concluded that CBS is likely to have heterogeneous causes (i.e., visual impairment, organic brain lesion, or both). It is, however, difficult to know the extent to which each of these potential causes contributes to the presence of CBS in individual patients. In the present study, the prevalence of CBS is investigated in the largest sample to date in this area of research, consisting of ophthalmologic and optometric patients.
2. Materials and method This study was undertaken at the Department of Ophthalmology, University of Occupational and Environmental Health, Kitakyushu city in Japan. One thousand consecutive new outpatients, including both low-vision and optometric patients, were examined by a questionnaire which consisted of ophthalmological questions as well as a question regarding the presence of visual hallucinations (i.e., ‘‘When people suffer from low visual acuity, they sometimes see things and/or other people that are not there. Has such phenomenon ever happened to you?’’). In order to assess the validity of the questionnaire, a separate group of 31 inpatients on the ophthalmologic ward were asked about the presence of visual hallucinations by using this questionnaire and again asked by a psychiatrist (YS) directly. As a result, 29 patients responded negatively both to the questionnaire and to direct questioning. One patient responded positively to both, and one provided conflicting responses by answering negatively to the questionnaire and positively to the direct question. Thus, the sensitivity and specificity were 50 and 100%, respectively. The positive predictive value and negative predictive value were 100 and 97%, respectively. Finally, the overall diagnostic power was 97%. The outpatients were 453 men and 547 women and their mean age was 51.3 (S.D.=21.9). The mean corrected visual acuity of the best eye was calculated to be 1.1 by using log MAR units. Of 1000 patients, there were 395 optometric patients and 605 patients with eye diseases. In the case of a positive answer to the question about visual hallucinations, the patients underwent a semistructured interview by a psychiatrist (YS) on visual hallucinations, and were interviewed using the Mini
International Neuropsychiatric Interview (MINI). The MINI was used for the exclusion of psychiatric disorders that may produce visual hallucinations. These interviews were performed after the patients’ informed consent to a further investigation was obtained. The semi-structured interview consisted of the following question: ‘‘When people have trouble with their eyes, it frequently affects their vision. It may make it difficult to see things that are there, but sometimes people see things that really are not there or see things that other people don’t see. Has this ever happened to you?’’ This question was derived from the article of Holroyd et al. (1994) in order to reconfirm the presence of visual hallucinations in our subjects. If the patient answered ‘yes’, then he/she was interviewed with special attention to the characteristics of visual hallucinations such as the recent frequency, the time of the day of occurrence, the duration, the laterality of the affected eye, the influence of eyelids, the emotional impact of the hallucinations on the patient, the content of visual hallucinations and insight into the unreal nature of the hallucinations. Most of these questions were derived from Teunisse et al. (1996). By using the above information, it was decided whether the individual patient had CBS according to Teunisse et al. (1996)’s CBS criteria as follows: at least one complex visual hallucination within the past 4 weeks; a period between the first and the last hallucination exceeding 4 weeks; full or partial retention of insight into the unreal nature of the hallucinations; absence of hallucinations in other sensory modalities; and absence of delusions. Since visual impairment and/or advanced age may be involved in CBS, subclass analyses were performed focusing on visual impairment and/or advanced age by using Fisher’s exact probability test.
3. Results On the screening questionnaire, 49 of 1000 (4.9%) patients answered positively. They were 23 males and 26 females with a mean age of 54.9 years (S.D.=15.7). Of these patients, 17 were optometric patients and 32 had eye diseases. All the optometric patients had visual impairment including ametropia (refractive error) (16 patients), and accommodation spasm (1 patient). Those with eye diseases included; cataract (14 patients), glaucoma (6 patients), diabetic retinopathy (4 patients), diabetic retinopathy plus cataract (2 patients) and others.
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When interviewed using the afore-mentioned semistructured interview by telephone or directly at the outpatient clinic of the university hospital, 23 patients denied their hallucinations because they marked ‘‘YES’’ by mistake. Two patients were lost to follow up. In the remaining 24 patients, 13 patients mistakenly answered positively due to mouches volantes (flying flies), three due to photopsia (dazzling), and eight patients (one man, seven women) actually suffered from complex visual hallucinations. Of these, three of the eight patients did not meet Teunisse et al. (1996)’s CBS criteria because one patient experienced the reappearance of letters and pictures just after having seen real ones, which was diagnosed as palinopsia. Another two patients had visual hallucinations only once or twice but not within the recent 4 weeks. Thus, only 5 of 1000 (0.5%) patients met Teunisse et al. (1996)’s CBS criteria. Moreover, none of the 5 patients had evidence of psychiatric disorder according to the results of MINI. As shown in Table 1, those who met criteria for CBS were all women with a mean age of 54.6 years (S.D.=17.3). The mean corrected visual acuity in the best eye was 0.43 in log MAR units. The most causes of visual impairment were ametropia. The characteristics of their visual hallucinations are also presented in Table 1. These characteristics were consistent with those described in Teunisse et al. (1996). There was no significant difference in age, gender ratio, or visual acuity between five CBS patients and the others. In subclass analyses, the prevalence of CBS was 3 of 372 (0.8%) in the low vision group (a visual acuity in the best eye of 0.3 or less), 2 of 346 (0.6%) in the elderly over 64 years of age, and 1 of 120 (0.8%) in both conditions. These prevalence did not significantly differ each other or from the overall one (0.5%).
4. Discussion The present results revealed low prevalence (0.5%) of CBS in a large cohort of ophthalmologic and optometric patients with relatively good visual acuity. This figure did not significantly increase even when the analyses were limited to patients with low visual acuity and/or old age. Thus, CBS seems to be a rare condition in patients with these particular characteristics. So far, the reported prevalence of CBS has been variable (Tables 2 and 3). Adachi (1996) diagnosed three cases of CBS in a cohort of 703 (0.4%) patients with leprosy and eye diseases and/or visual disturbances. Teunisse et al. (1995) revealed that 2 of 200 (1%) optometric patients had CBS. Berrios and Brook (1984) reported two cases with CBS of 150 (1.3%) referrals to a psychogeriatric service, and Norton-Willson and Munir (1987) showed eight patients with CBS of 434 (1.8%) referred to a psychogeriatric service. O’Reilly and Chamberlaine (1996) showed 7 of 200 (3.5%) elderly patients as suffering from CBS. These prevalences are relatively small. In contrast, Teunisse et al. (1995) reported 33 of 300 (11%) low-vision patients as suffering from CBS, and later Teunisse et al. (1996) showed 60 of 505 (12%) visually handicapped patients as having CBS. Olbrich et al. (1987) diagnosed 5 of 43 (12%) patients with severe visual impairment as CBS, and Nesher et al. (2001) reported that 11 of 89 (12%) glaucoma patients suffered from CBS. Brown and Murphy (1992) showed 12 CBS cases from a sample of 100 (12%) with choroidal neovascularization. These prevalences are substantially larger. Since all study locations of the high prevalence group involved ophthalmologic department and the percentage of visual impairment was 100% in this group (Table 2),
Table 1 Patient characteristics with Charles Bonnet syndrome Case Gender Age Visual acuity
Visual Frequency Time impairment
Duration State of eyelids
Emotion
Contents of visual hallucinations
Insight
Left (cor)a Right (cor) 1
Female 74
0.01 (0.01) 0.01 (0.01) Ametropia Unclear +cataract
Unclear 1–60 min Open and Indifference Purple insects moving in Present close a mass of black insects
2
Female 66
0.7 (1.0)
0.15 (0.4)
Ametropia Everyday
Evening 1–5 s
Open
Perplexed
A centipede moving on the wall or floor
Present
3
Female 61
0.6 (1.0)
0.6 (1.0)
Glaucoma
Unclear 1–5 s
Open
Anxious
A figure without movement
Present
4
Female 52
0.2 (0.5)
0.1 (1.2)
Ametropia Everyday
All day long
Open and Anxious close
Letters and a colourful landscape
Present
5
Female 29
0.2 (0.5)
0.15 (1.2)
Ametropia 1/2 weeks day time Unclear
Open
A walking figure in black Present
a
cor, corrected visual acuity.
Unclear
> 1h
Surprised
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Table 2 Prevalence studies of Charles Bonnet syndrome (CBS) Adachi (1996)
Berrios and Brook Norton-Willson (1984) and Munir (1987)
O’Reilly and Teunisse et al. Chamberlaine (1995) (1996)
Teunisse et al. (1996)
Olbrich et al. (1987)
Nesher et al. (2001)
Brown & Murphy (1992)
Study location Leprosarium
Department of opthalmology (optometry u.)
Psychogeriatic clinic
Psychogeriatric clinic
Psychiatric clinic
Department of ophthalmology (low vision u.)
Department of ophthalmology (low vision u.)
Department of ophthalmology
Department of ophthalmology (glaucoma u.)
Eye hospital (retina vascular u.)
Number of subjects
703
200
150
434
200
300
505
43
89
100
Gender
F=272, M=431
No data
F=103, M=47
No data
F=131, M=69
No data
No data
F=29, M=14
No data
F=75, M=25
Age (years)
68.6 (35–95)
above 64
77.0 (65–95)
65–95
Above 65
18–64 (N=79) above 64 (N=221)
Above 18
Above 65
No data
74.5 (41–90)
Visual impairment
Present (38%)
Present (30%)
Present (27%)
No data
No data
Present (100%) Present (100%) Present (100%) Present (100%) Present (100%)
Diagnostic criteria of CBS
VH+alert consciousness+ no mental disturbance
VH+insight to VH+no VH+absence underlying of delusions+ pathology no other hallucinations
u.=unit; VH, visual hallucinations.
No VH+full presentation orientation+ no psychiatric disorder+ insight to VH+ no other hallucinations
VH+insight to VH+absence of delusions+ no other hallucinations
VH+insight to VH+absence of delusions+ no other hallucinations
VH+insight to VH+no VH+absence dementia of delusions+ no other hallucinations
VH
Y. Shiraishi et al. / Journal of Psychiatric Research 38 (2004) 207–213
Teunisse et al. (1995)
Adachi (1996)
Teunisse et al. (1995)
Berrios and Brook (1984)
Norton-Willson and Munir (1987)
O’Reilly and Chamberlaine (1996)
Teunisse et al. (1995)
Teunisse et al. (1996)
Olbrich et al. (1987)
Nesher et al. (2001)
Brown & Murphy (1992)
Number of CBS (prevalence)
3 (0.4%)
2 (1%)
2 (1.3%)
8 (1.8%)
7 (3.5%)
33 (11%)
63 (12%)
5 (12%)
11 (12%)
12 (12%)
Gender
F=3, M=0
No data
No data
F=7, M=1
F=7, M=0
no data
F=42, M=18
F=3, M=2
F=3, M=8
F=11, M=1
Age (years)
77.0 (70–86)
No data
No data
83.8 (73–93)
80.9 (SD=8.6)
no data
75.4 (46–98; SD=8.0)
80.0 (69–88)
74.0 (60–96)
78.0 (73–87)
Visual impairment
Present (100%)
Present (50%)
No data
Present (100%)
Present (71%)
Present (100%)
Present (100%)
Present (100%)
Present (100%)
Present (100%)
Y. Shiraishi et al. / Journal of Psychiatric Research 38 (2004) 207–213
Table 3 Reported prevalence of Charles Bonnet syndrome
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visual impairment might have been associated with the increase of prevalence. With regard to the present study, although the study location was ophthalmologic and similar to previous studies that revealed high prevalence, the prevalence of CBS in our cohort (0.5%) was in line with previous studies that showed low prevalence. Taking visual acuity into consideration, the mean corrected visual acuity of the best eye of our 1000 patients was 1.1, whereas that of Teunisee et al. (1996)’s patients was 0.23 and Olbrich et al. (1987)’s patients had a visual acuity of less than 0.3 in the better eye. Moreover, Nesher et al. (2001)’s patients had a visual acuity of 0.25 or less in both eyes. Thus, the difference in prevalence between our study and that of other studies investigating ophthalmologic patients may be due to differences in the visual acuity of the cohort under investigation. Also, it seems likely that the lack of increased prevalence in our subclass analyses of the patients with low visual acuity was because the overall prevalence itself is very small (0.5%). As such, we cannot rule out the possibility that visual impairment (low visual acuity) may bring about CBS. In fact, interestingly, in our validation study of the questionnaire, we actually found a 6.45% prevalence ratio of visual hallucinations in ophthalmologic inpatients, thus attesting to the issues of severity of visual acuity and presence of ophthalmologic diagnoses influencing the rate of CBS. With regard to phenomenology of CBS, the characteristics observed in the present study were almost entirely consistent with Tuenisse et al. (1996). Also, Santhouse et al. (2000) showed that there were three clusters in the content of visual hallucinations: the first cluster consisted of hallucinations of extended landscape scenes and small figures in costumes with hats; the second, hallucinations of grotesque, disembodied and distorted faces with prominent eyes and teeth; and the third, visual perseveration and delayed palinopsia. In our cases with CBS, cases 1,3,5 belong to the first cluster and cases 2 and 4 are contained in the second cluster. Functional MRI findings have shown that the anterior ventral temporal lobes may be specialized for complex features related to hallucinations of objects and landscapes and that the superior temporal sulcus may be specialized for the distorted, grotesque faces with prominent staring eyes in the typical face hallucinations (Santhouse et al., 2000). Although we did not examine our subjects with functional MRI, it can be speculated that cases 1,3,5 may have been associated with the dysfunction of the anterior ventral temporal lobes and cases 2 and 4 with the superior temporal sulcus. There are methodological limitations in the present study. A questionnaire was used to determine the prevalence of CBS. Although the specificity of the questionnaire was 100%, the sensitivity was 50%. Notwithstanding this limitation, even when sensitivity is
taken into consideration, the prevalence of CBS in our patients seems still low. In conclusion, our findings suggest that the prevalence of CBS is low in patients with these particular characteristics and therefore this syndrome appears to be rare in even ophthalmologic and optometric patients if they do not have seriously low vision. Further studies are needed to investigate the prevalence of CBS in general population.
References Adachi N. Charles Bonnet syndrome in leprosy: prevalence and clinical characteristics. Acta Psychiatrica Scandinavica 1996;93: 279–81. Ball CJ. The vascular origins of the Charles Bonnet syndrome: four cases and a review of the pathogenic mechanisms. International Journal of Geriatric Psychiatry 1991;6:673–9. Berrios GE, Brook P. Visual hallucinations and sensory delusions in the elderly. British Journal of Psychiatry 1984;144:662–4. Brown GC, Murphy RP. Visual symptoms associated with choroidal neovascularization: photopsias and the Charles Bonnet syndrome. Archives of Ophthalmology 1992;110:1251–6. Damas-Mora J, Skelton-Robinson M, Jenner FA. The Charles Bonnet syndrome in perspective. Psychological Medicine 1982;12:251–61. Fernandez A, Lichtschein G, Vieweg WVR. The Charles Bonnet syndrome: a review. Journal of Nervous and Mental Disease 1997;185: 195–200. Gold K, Rabins PV. Isolated visual hallucinations and the Charles Bonnet syndrome: a review of the literature and presentation of six cases. Comprehensive Psychiatry 1989;30:90–8. Holroyd S, Rabins PV, Finkelstein D, Lavrisha M. Visual hallucinations in patients from an ophthalmology clinic and medical clinic population. Journal of Nervous and Mental Disease 1994;182:273–6. Nesher R, Nesher G, Epstein E, et al. Charles Bonnet syndrome in glaucoma patients with low vision. Journal of Glaucoma 2001;10: 396–400. Norton-Willson L, Munir M. Visual perceptual disorders resembling the Charles Bonnet syndrome: a study of 434 consecutive patients referred to a psychogeriatric unit. Family Practice 1987;4:27–31. Olbrich HM, Engelmeier MP, Pauleikhoff D, Assia E. Visual hallucinations in ophthalmology. Graefes Archive for Clinical and Experimental Ophthalmolology 1987;225:217–20. O’Reilly R, Chamberlaine C. Charles Bonnet syndrome: incidence and demographic and clinical features. Canadian Journal of Psychiatry 1996;41:259–60. Pliskin NH, Kiolbasa TA, Towle VL, Waubke T. Charles Bonnet syndrome: an early marker for dementia? Journal of American Geriatrics Society 1996;44:1055–61. Podoll K, Schwarz M, Noth J. Charles Bonnet-syndrome bei einem Parkinson Patienten mit Beidseitigem Visusverlust. Nervenarzt 1990;61:673–9. Santhouse AM, Howard RJ, Ffytche DH. Visual hallucinatory syndromes and the anatomy of the visual brain. Brain 2000;123: 2055–64. Terao T, Collinson S. Charles Bonnet syndrome and dementia. Lancet 2000;355:2168. Terao T. Hallucinations in Alzheimer’s disease and Charles Bonnet syndrome. American Journal of Psychiatry 2000a;157:2062. Terao T. Visual hallucinations in Alzheimer’s disease: possible involvement of low visual acuity and dementia with Lewy bodies. Journal of Neuropsychiatry and Clinical Neurosciences 2000b;12: 516–7.
Y. Shiraishi et al. / Journal of Psychiatric Research 38 (2004) 207–213 Terao T, Collinson S. Comments on ‘‘Treating Charles Bonnet syndrome: understanding inconsistency’’. Journal of Clinical Psychopharmacology 2001;21:164–6. Terao T. The present state of Charles Bonnet syndrome. Psychogeriatrics 2002;2:6–14. Teunisse RJ, Cruysberg JRM, Verbeek A, Zitman FG. The Charles
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Bonnet syndrome: a large prospective study in the Netherlands. British Journal of Psychiatry 1995;166:254–7. 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.
The rarity of Charles Bonnet syndrome Yasuko Shiraishia, Takeshi Teraoa,*, Kenji Ibib, Jun Nakamuraa, Akihiko Tawarab a Department of Psychiatry, University of Occupational and Environmental Health School of Medicine, Kitakyushu, Japan Department of Opthalmology, University of Occupational and Environmental Health School of Medicine, Kitakyushu, Japan
b
Received 11 November 2002; received in revised form 7 May 2003; accepted 11 June 2003
Abstract Charles Bonnet syndrome (CBS) is characterized by complex visual hallucinations in otherwise psychologically normal people. Estimates of the prevalence of CBS in different samples vary from a small percentage (around 1%), to a relatively large percentage (about 10%). The purpose of the present study is to determine whether CBS is rare or not. One-thousand ophthalmologic and optometric outpatients at a university hospital were consecutively screened by a questionnaire to identify patients possibly experiencing visual hallucinations. The mean corrected visual acuity in the best eye was 1.1. Those who positively responded to the questionnaire were further investigated to determine whether their symptoms were consistent with CBS. As a result, the prevalence of CBS was 0.5% (5/1000). In subclass analyses, the prevalence was 3 of 372 (0.8%) in the low vision group, 2 of 346 (0.6%) in the elderly, and 1 of 120 (0.8%) in both conditions. These were not significantly different from each other or from the overall prevalence (0.5%). This low prevalence of CBS in our subjects may be due to their relatively good visual acuity because previous studies with high prevalence of CBS investigated patients with a visual acuity of less than 0.3. The prevalence of CBS may be low in patients with these particular characteristics, and this syndrome seems to be rare in even ophthalmologic and optometric patients if they do not have seriously low vision. Further studies are needed to investigate the prevalence of CBS in general population. # 2003 Elsevier Ltd. All rights reserved. Keywords: Charles Bonnet syndrome; Visual hallucinations; Visual acuity; Advanced age; Prevalence
1. Introduction Charles Bonnet syndrome (CBS) was named after the Swiss Philosopher who first described the occurrence of vivid complex visual hallucinations in his visually impaired, otherwise psychologically normal, grandfather Charles Lullin in 1760 (Damas-Mora et al., 1982). Since then, the disorder has been widely reported but estimates of prevalence vary considerably from study to study from as low as 0.4% (Adachi, 1996) to as high as 12% (Teunisse et al., 1996). As such, it is presently uncertain whether CBS is rare or not. An explanation for differences in the reported prevalence of CBS may lie in the different diagnostic criteria applied and the samples used to investigate the disorder. There have been five sets of diagnostic criteria (Damas-Mora et al., 1982; Teunisse et al., 1996; Gold * Corresponding author. Tel.: +81-93-691-7253; fax: +81-93-6924894. E-mail address: [email protected] (T. Terao). 0022-3956/$ - see front matter # 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0022-3956(03)00090-6
and Rabins, 1989; Podoll et al., 1990; Ball, 1991) for CBS and, with the exception of Ball (1991), all included the presence of insight to visual hallucinations; thus ‘‘psychological normality’’ may be at least partially guaranteed in CBS patients (Terao and Collinson, 2001; Terao, 2002). In addition, the above-mentioned criteria do not require the presence of optic pathology, although clinicians commonly associate CBS with eye diseases (Fernandez et al., 1997). Thus, low visual acuity is not necessary for diagnosing CBS, but there remains a possibility that in some CBS patients low visual acuity may actually bring about visual hallucinations. In any case, these criteria seem to be relatively consistent in diagnosing visual hallucinations in otherwise psychologically normal people but have nevertheless been applied to a range of very different samples from ophthalmologic patients to psychogeriatric patients (Terao, 2002). Another possible reason for differences in the reported prevalence of CBS is that all of the abovementioned diagnostic criteria have been derived almost exclusively from cross-sectional observations. It is therefore
208
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possible that some patients with dementia manifest complex visual hallucinations in the early stages of the illness and they may be inappropriately diagnosed as suffering from CBS (Terao & Collinson, 2000; Pliskin et al., 1996). Conversely, it is also possible that visual hallucinations in patients with dementia may be not only due to dementia itself, but also due to CBS (Terao, 2000a,b). Recently, Terao (2002) reviewed the pertinent references to CBS, and concluded that CBS is likely to have heterogeneous causes (i.e., visual impairment, organic brain lesion, or both). It is, however, difficult to know the extent to which each of these potential causes contributes to the presence of CBS in individual patients. In the present study, the prevalence of CBS is investigated in the largest sample to date in this area of research, consisting of ophthalmologic and optometric patients.
2. Materials and method This study was undertaken at the Department of Ophthalmology, University of Occupational and Environmental Health, Kitakyushu city in Japan. One thousand consecutive new outpatients, including both low-vision and optometric patients, were examined by a questionnaire which consisted of ophthalmological questions as well as a question regarding the presence of visual hallucinations (i.e., ‘‘When people suffer from low visual acuity, they sometimes see things and/or other people that are not there. Has such phenomenon ever happened to you?’’). In order to assess the validity of the questionnaire, a separate group of 31 inpatients on the ophthalmologic ward were asked about the presence of visual hallucinations by using this questionnaire and again asked by a psychiatrist (YS) directly. As a result, 29 patients responded negatively both to the questionnaire and to direct questioning. One patient responded positively to both, and one provided conflicting responses by answering negatively to the questionnaire and positively to the direct question. Thus, the sensitivity and specificity were 50 and 100%, respectively. The positive predictive value and negative predictive value were 100 and 97%, respectively. Finally, the overall diagnostic power was 97%. The outpatients were 453 men and 547 women and their mean age was 51.3 (S.D.=21.9). The mean corrected visual acuity of the best eye was calculated to be 1.1 by using log MAR units. Of 1000 patients, there were 395 optometric patients and 605 patients with eye diseases. In the case of a positive answer to the question about visual hallucinations, the patients underwent a semistructured interview by a psychiatrist (YS) on visual hallucinations, and were interviewed using the Mini
International Neuropsychiatric Interview (MINI). The MINI was used for the exclusion of psychiatric disorders that may produce visual hallucinations. These interviews were performed after the patients’ informed consent to a further investigation was obtained. The semi-structured interview consisted of the following question: ‘‘When people have trouble with their eyes, it frequently affects their vision. It may make it difficult to see things that are there, but sometimes people see things that really are not there or see things that other people don’t see. Has this ever happened to you?’’ This question was derived from the article of Holroyd et al. (1994) in order to reconfirm the presence of visual hallucinations in our subjects. If the patient answered ‘yes’, then he/she was interviewed with special attention to the characteristics of visual hallucinations such as the recent frequency, the time of the day of occurrence, the duration, the laterality of the affected eye, the influence of eyelids, the emotional impact of the hallucinations on the patient, the content of visual hallucinations and insight into the unreal nature of the hallucinations. Most of these questions were derived from Teunisse et al. (1996). By using the above information, it was decided whether the individual patient had CBS according to Teunisse et al. (1996)’s CBS criteria as follows: at least one complex visual hallucination within the past 4 weeks; a period between the first and the last hallucination exceeding 4 weeks; full or partial retention of insight into the unreal nature of the hallucinations; absence of hallucinations in other sensory modalities; and absence of delusions. Since visual impairment and/or advanced age may be involved in CBS, subclass analyses were performed focusing on visual impairment and/or advanced age by using Fisher’s exact probability test.
3. Results On the screening questionnaire, 49 of 1000 (4.9%) patients answered positively. They were 23 males and 26 females with a mean age of 54.9 years (S.D.=15.7). Of these patients, 17 were optometric patients and 32 had eye diseases. All the optometric patients had visual impairment including ametropia (refractive error) (16 patients), and accommodation spasm (1 patient). Those with eye diseases included; cataract (14 patients), glaucoma (6 patients), diabetic retinopathy (4 patients), diabetic retinopathy plus cataract (2 patients) and others.
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When interviewed using the afore-mentioned semistructured interview by telephone or directly at the outpatient clinic of the university hospital, 23 patients denied their hallucinations because they marked ‘‘YES’’ by mistake. Two patients were lost to follow up. In the remaining 24 patients, 13 patients mistakenly answered positively due to mouches volantes (flying flies), three due to photopsia (dazzling), and eight patients (one man, seven women) actually suffered from complex visual hallucinations. Of these, three of the eight patients did not meet Teunisse et al. (1996)’s CBS criteria because one patient experienced the reappearance of letters and pictures just after having seen real ones, which was diagnosed as palinopsia. Another two patients had visual hallucinations only once or twice but not within the recent 4 weeks. Thus, only 5 of 1000 (0.5%) patients met Teunisse et al. (1996)’s CBS criteria. Moreover, none of the 5 patients had evidence of psychiatric disorder according to the results of MINI. As shown in Table 1, those who met criteria for CBS were all women with a mean age of 54.6 years (S.D.=17.3). The mean corrected visual acuity in the best eye was 0.43 in log MAR units. The most causes of visual impairment were ametropia. The characteristics of their visual hallucinations are also presented in Table 1. These characteristics were consistent with those described in Teunisse et al. (1996). There was no significant difference in age, gender ratio, or visual acuity between five CBS patients and the others. In subclass analyses, the prevalence of CBS was 3 of 372 (0.8%) in the low vision group (a visual acuity in the best eye of 0.3 or less), 2 of 346 (0.6%) in the elderly over 64 years of age, and 1 of 120 (0.8%) in both conditions. These prevalence did not significantly differ each other or from the overall one (0.5%).
4. Discussion The present results revealed low prevalence (0.5%) of CBS in a large cohort of ophthalmologic and optometric patients with relatively good visual acuity. This figure did not significantly increase even when the analyses were limited to patients with low visual acuity and/or old age. Thus, CBS seems to be a rare condition in patients with these particular characteristics. So far, the reported prevalence of CBS has been variable (Tables 2 and 3). Adachi (1996) diagnosed three cases of CBS in a cohort of 703 (0.4%) patients with leprosy and eye diseases and/or visual disturbances. Teunisse et al. (1995) revealed that 2 of 200 (1%) optometric patients had CBS. Berrios and Brook (1984) reported two cases with CBS of 150 (1.3%) referrals to a psychogeriatric service, and Norton-Willson and Munir (1987) showed eight patients with CBS of 434 (1.8%) referred to a psychogeriatric service. O’Reilly and Chamberlaine (1996) showed 7 of 200 (3.5%) elderly patients as suffering from CBS. These prevalences are relatively small. In contrast, Teunisse et al. (1995) reported 33 of 300 (11%) low-vision patients as suffering from CBS, and later Teunisse et al. (1996) showed 60 of 505 (12%) visually handicapped patients as having CBS. Olbrich et al. (1987) diagnosed 5 of 43 (12%) patients with severe visual impairment as CBS, and Nesher et al. (2001) reported that 11 of 89 (12%) glaucoma patients suffered from CBS. Brown and Murphy (1992) showed 12 CBS cases from a sample of 100 (12%) with choroidal neovascularization. These prevalences are substantially larger. Since all study locations of the high prevalence group involved ophthalmologic department and the percentage of visual impairment was 100% in this group (Table 2),
Table 1 Patient characteristics with Charles Bonnet syndrome Case Gender Age Visual acuity
Visual Frequency Time impairment
Duration State of eyelids
Emotion
Contents of visual hallucinations
Insight
Left (cor)a Right (cor) 1
Female 74
0.01 (0.01) 0.01 (0.01) Ametropia Unclear +cataract
Unclear 1–60 min Open and Indifference Purple insects moving in Present close a mass of black insects
2
Female 66
0.7 (1.0)
0.15 (0.4)
Ametropia Everyday
Evening 1–5 s
Open
Perplexed
A centipede moving on the wall or floor
Present
3
Female 61
0.6 (1.0)
0.6 (1.0)
Glaucoma
Unclear 1–5 s
Open
Anxious
A figure without movement
Present
4
Female 52
0.2 (0.5)
0.1 (1.2)
Ametropia Everyday
All day long
Open and Anxious close
Letters and a colourful landscape
Present
5
Female 29
0.2 (0.5)
0.15 (1.2)
Ametropia 1/2 weeks day time Unclear
Open
A walking figure in black Present
a
cor, corrected visual acuity.
Unclear
> 1h
Surprised
210
Table 2 Prevalence studies of Charles Bonnet syndrome (CBS) Adachi (1996)
Berrios and Brook Norton-Willson (1984) and Munir (1987)
O’Reilly and Teunisse et al. Chamberlaine (1995) (1996)
Teunisse et al. (1996)
Olbrich et al. (1987)
Nesher et al. (2001)
Brown & Murphy (1992)
Study location Leprosarium
Department of opthalmology (optometry u.)
Psychogeriatic clinic
Psychogeriatric clinic
Psychiatric clinic
Department of ophthalmology (low vision u.)
Department of ophthalmology (low vision u.)
Department of ophthalmology
Department of ophthalmology (glaucoma u.)
Eye hospital (retina vascular u.)
Number of subjects
703
200
150
434
200
300
505
43
89
100
Gender
F=272, M=431
No data
F=103, M=47
No data
F=131, M=69
No data
No data
F=29, M=14
No data
F=75, M=25
Age (years)
68.6 (35–95)
above 64
77.0 (65–95)
65–95
Above 65
18–64 (N=79) above 64 (N=221)
Above 18
Above 65
No data
74.5 (41–90)
Visual impairment
Present (38%)
Present (30%)
Present (27%)
No data
No data
Present (100%) Present (100%) Present (100%) Present (100%) Present (100%)
Diagnostic criteria of CBS
VH+alert consciousness+ no mental disturbance
VH+insight to VH+no VH+absence underlying of delusions+ pathology no other hallucinations
u.=unit; VH, visual hallucinations.
No VH+full presentation orientation+ no psychiatric disorder+ insight to VH+ no other hallucinations
VH+insight to VH+absence of delusions+ no other hallucinations
VH+insight to VH+absence of delusions+ no other hallucinations
VH+insight to VH+no VH+absence dementia of delusions+ no other hallucinations
VH
Y. Shiraishi et al. / Journal of Psychiatric Research 38 (2004) 207–213
Teunisse et al. (1995)
Adachi (1996)
Teunisse et al. (1995)
Berrios and Brook (1984)
Norton-Willson and Munir (1987)
O’Reilly and Chamberlaine (1996)
Teunisse et al. (1995)
Teunisse et al. (1996)
Olbrich et al. (1987)
Nesher et al. (2001)
Brown & Murphy (1992)
Number of CBS (prevalence)
3 (0.4%)
2 (1%)
2 (1.3%)
8 (1.8%)
7 (3.5%)
33 (11%)
63 (12%)
5 (12%)
11 (12%)
12 (12%)
Gender
F=3, M=0
No data
No data
F=7, M=1
F=7, M=0
no data
F=42, M=18
F=3, M=2
F=3, M=8
F=11, M=1
Age (years)
77.0 (70–86)
No data
No data
83.8 (73–93)
80.9 (SD=8.6)
no data
75.4 (46–98; SD=8.0)
80.0 (69–88)
74.0 (60–96)
78.0 (73–87)
Visual impairment
Present (100%)
Present (50%)
No data
Present (100%)
Present (71%)
Present (100%)
Present (100%)
Present (100%)
Present (100%)
Present (100%)
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Table 3 Reported prevalence of Charles Bonnet syndrome
211
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visual impairment might have been associated with the increase of prevalence. With regard to the present study, although the study location was ophthalmologic and similar to previous studies that revealed high prevalence, the prevalence of CBS in our cohort (0.5%) was in line with previous studies that showed low prevalence. Taking visual acuity into consideration, the mean corrected visual acuity of the best eye of our 1000 patients was 1.1, whereas that of Teunisee et al. (1996)’s patients was 0.23 and Olbrich et al. (1987)’s patients had a visual acuity of less than 0.3 in the better eye. Moreover, Nesher et al. (2001)’s patients had a visual acuity of 0.25 or less in both eyes. Thus, the difference in prevalence between our study and that of other studies investigating ophthalmologic patients may be due to differences in the visual acuity of the cohort under investigation. Also, it seems likely that the lack of increased prevalence in our subclass analyses of the patients with low visual acuity was because the overall prevalence itself is very small (0.5%). As such, we cannot rule out the possibility that visual impairment (low visual acuity) may bring about CBS. In fact, interestingly, in our validation study of the questionnaire, we actually found a 6.45% prevalence ratio of visual hallucinations in ophthalmologic inpatients, thus attesting to the issues of severity of visual acuity and presence of ophthalmologic diagnoses influencing the rate of CBS. With regard to phenomenology of CBS, the characteristics observed in the present study were almost entirely consistent with Tuenisse et al. (1996). Also, Santhouse et al. (2000) showed that there were three clusters in the content of visual hallucinations: the first cluster consisted of hallucinations of extended landscape scenes and small figures in costumes with hats; the second, hallucinations of grotesque, disembodied and distorted faces with prominent eyes and teeth; and the third, visual perseveration and delayed palinopsia. In our cases with CBS, cases 1,3,5 belong to the first cluster and cases 2 and 4 are contained in the second cluster. Functional MRI findings have shown that the anterior ventral temporal lobes may be specialized for complex features related to hallucinations of objects and landscapes and that the superior temporal sulcus may be specialized for the distorted, grotesque faces with prominent staring eyes in the typical face hallucinations (Santhouse et al., 2000). Although we did not examine our subjects with functional MRI, it can be speculated that cases 1,3,5 may have been associated with the dysfunction of the anterior ventral temporal lobes and cases 2 and 4 with the superior temporal sulcus. There are methodological limitations in the present study. A questionnaire was used to determine the prevalence of CBS. Although the specificity of the questionnaire was 100%, the sensitivity was 50%. Notwithstanding this limitation, even when sensitivity is
taken into consideration, the prevalence of CBS in our patients seems still low. In conclusion, our findings suggest that the prevalence of CBS is low in patients with these particular characteristics and therefore this syndrome appears to be rare in even ophthalmologic and optometric patients if they do not have seriously low vision. Further studies are needed to investigate the prevalence of CBS in general population.
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