J Neurol Neurosurg Psychiatry 2001;70:727–733 727 Visual hallucinations in Parkinson’s disease: a review and phenomenological survey J Barnes, A S David Abstract According to the DSM IV criteria,1 a hallucina- Objectives—Between 8% and 40% of pa- tion is “a sensory perception without external tients with Parkinson’s disease undergo- stimulation of the relevant sensory organ” dis- ing long term treatment will have visual tinguishing it from an illusion, in which an hallucinations during the course of their external stimulus is perceived but then misin- illness. There were two main objectives: terpreted. Although separate, the phenomena firstly, to review the literature on Parkin- often overlap, with illusions leading to halluci- son’s disease and summarise those factors nations and vice versa. One of the commonest most often associated with hallucinations; neurological conditions associated with visual secondly, to carry out a clinical compari- hallucinations is Parkinson’s disease. Although son of ambulant patients with Parkinson’s there are reports of visual hallucinations in disease with and without visual hallucina- Parkinson’s disease before the dopamine era,2 tions, and provide a detailed phenomeno- the phenomena have only been noted as a fre- logical analysis of the hallucinations. quent complication of the disorder since Methods—A systematic literature search levodopa treatment was introduced.3 using standard electronic databases of One categorisation of visual hallucinations is published surveys and case-control stud- “simple” versus “complex”. Simple hallucina- ies was undertaken. In parallel, a two stage tions are characterised by the absence of form, questionnaire survey was carried out and are often photopsias such as flashes of light based on members of a local branch of the or colour. Occasionally, geometric shapes are Parkinson’s Disease Society and followed described which move around in space. up with a clinical interview. Complex visual hallucinations are character- Results—The review disclosed common ised by visions that are clearly defined, have factors associated with visual hallucina- specific form, and can include animals, objects, tions in Parkinson’s disease including and humans. These two types tend to be seen greater age and duration of illness, cogni- as having localisation value: simple, pointing to 45 tive impairment, and depression and sleep occipital pathology whereas the complex type 67 disturbances. The survey comprised 21 are presumed to involve the temporal cortex, patients with visual hallucinations and 23 either directly or indirectly through modula- without. The hallucinators had a longer tory connections (as in peduncular hallucino- sis).910 duration and a greater severity of illness, 11 and tended to show more depressed mood In a recent review it was proposed that and cognitive impairment. The typical there were three basic mechanisms, which, visual hallucination in these patients is a alone or in combination, underlie complex complex visual image experienced while visual hallucinations with widely diVering they are alert and have their eyes open. causes: irritative processes acting on higher visual centres or pathways; defective visual Department of The image appears without any known Psychology, Oxford trigger or voluntary eVort, is somewhat processing (both peripheral and central); and Brookes University, blurred, and commonly moves. It stays brainstem modulation of thalamocortical con- Gipsy Lane, present for a period of “seconds” or nections. Headington, Oxford “minutes”. The content can be variable In this article we review surveys of visual OX3 0BP,UK hallucinations in patients with Parkinson’s dis- J Barnes within and between hallucinators, and ASDavid includes such entities as people, animals, ease and contribute a survey of our own. The buildings, or scenery. These features re- objectives were firstly, to characterise the typi- Division of semble those highlighted in hallucinations cal features of the hallucinations in Parkinson’s Psychological in the visually impaired (Charles Bonnet’s disease and summarise their associations; and Medicine, Section of secondly, to compare these findings to those Cognitive syndrome). Conclusion—A consistent set of factors derived from descriptions of visual hallucina- Neuropsychiatry, GKT tions in other disorders. The aim was to exam- School of Medicine are associated with visual hallucinations and Institute of in Parkinson’s disease. The results of the ine whether the phenomena in diVerent Psychiatry, London phenomenological survey and those of settings have characteristics in common despite SE5 8AF, UK visual hallucinations carried out in other varied causes and whether inferences about J Barnes settings suggest a common physiological their pathophysiology can be made on this basis. Correspondence to: substrate for visual hallucinations but Professor A S David with cognitive factors playing an as yet [email protected] unspecified role. (J Neurol Neurosurg Psychiatry 2001;70:727–733) Literature review Received 15 May 2000 and A systematic literature search using in final form 6 November 2000 Keywords: visual hallucinations; Parkinson’s disease; MEDLINE and EMBASE databases was Accepted 22 November 2000 phenomenology carried out on papers published in English www.jnnp.com 728 Barnes, David between 1966 and December 1999. Search terms were Parkinson(s) and hallucination(s)/ and “visual”. Case series, surveys, and case- control studies were included, but not case reports and reviews. The minimum quality cri- erent terion was some information on how the diag- V nosis of Parkinson’s disease was reached and qualitative information on abnormal visual duration matched controls v phenomena. These criteria excluded most periods V halls Comments studies including those before 1990 (thor- o MMSE fell over follow up;measures CT not di bromocriptine in VH-ve group and visual hallucinations here). Formed VH occurred in 48 (22% of whole sample) oughly reviewed by Cummings.3 Table 1 sum- maries the results of included studies published after 1991. Sleep disturbance ? Emphasis on combined auditory Prevalence Prevalence rates of 11/89 (12.3%) for visual illusions plus hallucinations,12 or 23/189 (11.6%) for hallucinations13 are typical of sam- ples of chronically treated patients. Recent sur- veys give prevalence estimates of visual halluci- nations between 8.8% and 44%.14–19 The visual phenomena range from bizarre, complex, and Less in late onsetgroup only) ? Main analysis early/late onset of frightening “visions”, through distortions of real percepts (illusions) to vague feelings of a “presence”. Aarsland et al20 carried out a com- munity based study of 235 patients in Norway with Parkinson’s disease. Of these, 23 patients (9.8%) had hallucinations with retained in- Disease severity/ disability Depression sight, and another 14 patients (6%) had more + motor disorder in early onset severe hallucinations and delusions. Under- reporting is a possible problem,15 even in inter- view studies, possibly because patients may fear being labelled as “mad”. Cognitive impairment + late onset only Risk factors The review—based on a total of 316 hallucina- tors and 806 comparison subjects— showed consistent results in terms of risk factors for agonists visual hallucinations (table 1). Some features such as visual impairment have been found to be associated with visual hallucinations in gen- eral21 and in other neurological disorders.22 Pri- mary deficits in visual processing are associated Association with visual hallucinations with Parkinson’s disease and have been exhaus- Age Duration Medication dose tively reviewed elsewhere.23 The possible link with sleep disturbances has also been discussed at length.11 24 MEDICATION Comparisons of hallucinators and non- hallucinators have seldom shown major diVer- ences in drug history.16 Anticholinergic agents may be responsible for confusion in elderly people25 and cholinergic26 and serotonergic systems together have been implicated in hallucinations.27 Some authors noted increased use of anticholinergic drugs (and primary Controls/ comparison group Sample dopamine agonists) but the results are incon- sistent. Goetz et al28 studied five non-demented patients with Parkinson’s disease with daily No of patients 10Aud +VH hallucinations who were given high dose 301629 2055 2032 58 Random clinical35 214 Clinic survey: initial mailing23 Prospective clinical86 + 97 Consecutive + clinical 76 − * 212 − Clinic survey 109 + Consecutive clinical * − Population based − − Consecutive clinical − − ? + − + + + Trend + + − + dopamine − + (lifetime) + + +/− − + − + + + + − − (when adjusted for age) − ? + − + + (history) + (reported in AH+VH Not premorbid IQ − + + + + 8 patients’ VHs associated with Higher anticholinergic and *Matched for age/duration. + + 21 had auditory (not First included population based study 15 levodopa infusions in a placebo controlled trial. 29 53 20 17 No hallucinations were provoked. Fernandez et 19 et al 1992 29 31 1998 al found that when there was an apparent link 1999 1997 2000 et al between hallucinations and medication or 1997 et al et al et al et al clinical state it was more likely to be in periods 16 of immobility. Hence visual hallucinations do et al 1996 Inzelberg Study Fernandez Sanchez-Ramos Graham Aarsland Klein Fenelon Table 1 Summary of studies of visual hallucinations in Parkinson’s patients with disease showing clinical associations not simply relate to high levels of dopaminergic Haeske-Dewick 1995 +=Definite