Early and Presenting Symptoms of Dementia with Lewy Bodies

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1 Original Research Article DOI: / Accepted: September 6, 2011 Published online: November 16, 2011 Early and Presenting Symptoms of Dementia with Lewy Bodies Eirik Auning a Arvid Rongve c Tormod Fladby b Jan Booij e Tibor Hortobágyi f, i Françoise J. Siepel d Clive Ballard g Dag Aarsland d, h, j Departments of a Geriatric Psychiatry and b Neurology, Akershus University Hospital, Lorenskog, c Department of Psychiatry, Haugesund Hospital, Haugesund, and d Department of Geriatric Psychiatry, Psychiatric Clinic, Stavanger University Hospital, Stavanger, Norway; e Department of Nuclear Medicine, University of Amsterdam, Academic Medical Center, Amsterdam, The Netherlands; f Department of Clinical Neuroscience, Institute of Psychiatry, and g Wolfson Centre for Age-Related Diseases, King s College London, London, UK; h NVS Department, KI Alzheimer Disease Research Center, Karolinska Institutet, Novum, Stockholm, Sweden; i Department of Neuropathology, Institute of Pathology, University of Debrecen, Debrecen, Hungary; j University of Oslo, Ahus Campus, Oslo, Norway Key Words Dementia with Lewy bodies Alzheimer s disease dementia Parkinsonism Predementia Carer report Abstract Background/Aims: To explore the presenting and early symptoms of dementia with Lewy bodies (DLB). Method: Patients with mild dementia fulfilling diagnostic criteria for DLB (n = 61) and Alzheimer s disease (AD) (n = 109) were recruited from outpatient dementia clinics in western Norway. At diagnosis, caregivers were asked which symptom had been the presenting symptom of dementia. Results: Caregivers reported that memory impairment was the most common presenting symptom in DLB (57%), followed by visual hallucinations (44%), depression (34%), problem solving difficulties (33%), gait problems (28%), and tremor/stiffness (25%). In contrast, 99% of AD carers reported impaired memory as a presenting symptom, whereas visual hallucinations were a presenting symptom in 3% of the AD cases. Conclusion: DLB should be suspected in predementia cases with visual hallucinations. Copyright 2011 S. Karger AG, Basel Introduction Dementia with Lewy bodies (DLB) is the second most common cause of neurodegenerative dementia and accounts for 15 20% of cases [1, 2]. DLB has a more malignant course in terms of the rate of cognitive decline, mortality, quality of life, and medical costs compared to Alzheimer s disease (AD) [3 5]. However, in contrast to the increasing focus on early stage AD and Parkinson s disease (PD), very few studies have explored the initial presentation of DLB, and the clinical phenotype of the predementia stage of DLB is essentially unexplored. Thus more information is needed for early diagnosis of DLB. There is, however, evidence that DLB is the common end stage of a variety of clinical pathways, emerging from disorders of sleep such as REM sleep behavioral disorder (RBD), parkinsonism, primary autonomic dysfunction, and visual hallucinations as well as mild cognitive impairment (MCI). Several studies have shown that a substantial proportion of people with idiopathic RBD will subsequently develop dementia with cortical Lewy bodies [6]. A recent prospective study showed that 40% of patients with idiopathic RBD have nigral pathology and Fax S. Karger AG, Basel /11/ $38.00/0 Accessible online at: Dag Aarsland NVS Department, KI Alzheimer Disease Research Center Karolinska Institutet, Novum SE Stockholm (Sweden) Tel , gmail.com

2 decreased striatal dopamine transporters as demonstrated by SPECT imaging and that such changes are associated with an increased risk of developing DLB [7]. A clinicopathological study of 8 patients diagnosed with MCI during life who had DLB at autopsy suggests that RBD can be a first feature of DLB, followed by parkinsonism and cognitive impairment. Visual hallucinations usually occurred after cognitive impairment, although cases with early hallucinations were reported, whereas fluctuating cognition seems to occur late in DLB [8]. In another clinicopathological study, MCI patients who subsequently developed DLB were more impaired on executive functioning and mental speed tests and less impaired on some memory measures compared to those who later developed AD. In addition, noncognitive features such as delirium and visual hallucinations were more common at an early disease stage in these patients [9]. This distinctive cognitive profile in predementia DLB was also confirmed by another study [8]. In DLB, autonomic symptoms such as orthostatic hypotension and falls are particularly common [10] and pure autonomic failure (PAF) can also be the clinical presentation of DLB [6, 11]. Brain changes characteristic of cortical Lewy body disease, such as loss of dopamine transporters [12] and reduced perfusion of the anterior cingulate and medial frontal lobe [13], have been reported in PAF, supporting the hypothesis that DLB may present clinically with PAF. Finally, the majority of patients with PD will eventually develop dementia associated with PD (PDD) [14], a syndrome with a pathological and clinical phenotype indistinguishable from DLB [15]. Thus, there are several possible clinical starting points and trajectories with a common final pathological and clinical syndrome of cortical Lewy body disease. Identifying and characterizing the first stage of DLB is important in order to plan optimal management, to gain insight into early mechanisms of disease development, and to distinguish DLB from early stage AD [16]. Emerging evidence underlines the importance of expanding the characterization of the dementing disorders beyond cognition [8]. The objective of this retrospective study therefore was to describe the presenting clinical symptoms of 61 patients with DLB. Subjects and Methods Subjects From March 2005 to March 2007, we screened all referrals in five outpatient clinics of geriatric medicine and old age psychiatry in the counties of Rogaland and Hordaland in western Norway with a first time diagnosis of dementia according to the Diagnostic and Statistical Manual for Mental Disorders, 4th edition (DSM-IV). Patients with a Mini-Mental State Examination (MMSE) score of 20 or more were included to ascertain only mild dementia cases. The three neurology outpatient clinics in the area agreed to refer all new dementia cases to one of the participating centers. From 2007, we consecutively recruited patients with DLB and PDD. A study physician performed a structured clinical interview to ascertain demographics, previous diseases, drug history and conducted a clinical examination. Routine blood tests and MRI were performed in all patients. Dopamine transporter imaging ( 123 I-FP-CIT SPECT) was performed [17, 18], but due to limited resources it was only done in 33 patients with suspected DLB. Patients with acute delirium or confusion, terminal illness, a recently diagnosed major somatic illness, previous bipolar disorder or a psychotic disorder were excluded. Only subjects with AD or DLB were included in this study. Seventeen of 61 DLB patients and 68 of 109 AD patients were recruited from the department of geriatrics; the rest were from the department of old age psychiatry. Ethical Permission The study was approved by the regional ethics committee and the Norwegian authorities for the collection of medical data. The patients provided written informed consent to participate in and withdraw at any stage from the study after the procedures had been explained in detail to the patient and a caregiver, usually the spouse or offspring. Dementia Diagnosis As previously described in more detail [2], patients were diagnosed as having AD according to the National Institute of Neurological and Communicative Disorders and Stroke-Alzheimer s Disease and Related Disorders Association (NINCDS-ADRDA) [19], DLB according to the revised consensus criteria [1] and PDD was differentiated from DLB using the 1-year rule as recommended by the task force organized by the Movement Disorder Society [15, 20]. Only AD and DLB patients were included in this study. In addition to the clinical examination, the dementia diagnosis was based on a standardized carer questionnaire, cognitive testing including MMSE, and a neuropsychological battery including tests of verbal memory, attention, executive and visuospatial functioning, and language [2]. Diagnosis was determined by two research clinicians after all clinical and imaging information was available. Patients were recruited for autopsy, and currently 5 have a pathological diagnosis, 3 AD, 1 DLB, and 1 frontotemporal dementia, all in accordance with clinical diagnosis. Clinical and Imaging Assessments Core and Suggestive Features of DLB Standardized clinical rating scales were applied to identify the core and suggestive DLB features based on cutoff values for significant symptom severity as recommended in the original papers (see below) or based on a previous study from our group [21]. Visual hallucinations and other psychiatric symptoms were assessed using the Neuropsychiatric Inventory (NPI) [22], a structured, carer-based clinical interview covering 12 psychiatric symptoms commonly occurring in people with dementia, including halluci- Early and Presenting Symptoms of DLB 203

3 Table 1. Demographics and clinical characteristics at the time of diagnosis Variables DLB (n = 61) AD (n = 109) p value Age, years (54 92) (50 90) Female sex, n 26 (42.6%) 82 (75.2%) MMSE score (16 28) (19 29) Education, years (7 19) (4 18) UPDRS III total score (0 53) (0 9) Median NPI total score (range) (0 89) 8.00 (0 63) Disease duration, years (0 10) (0 10) N umbers represent means 8 standard deviation (range) unless otherwise indicated. The two groups did not differ regarding age or years of education. The DLB group had a slightly longer disease duration, contained more males, and had higher UPDRS motor and NPI total scores. In addition, DLB patients had slightly lower MMSE scores compared to the AD group. UPDRS III = Unified Parkinson s disease rating scale. nations. NPI item 2 (hallucinations) was further explored for different modalities to ensure a high specificity for visual hallucinations. Fluctuating cognition was rated using the Clinician Assessment of Cognitive Fluctuations [23] or the Mayo Fluctuation Scale [24] with recommended cutoff values of 4/5 and 3/4, respectively. RBD was assessed using the Mayo Sleep Questionnaire, a structured and validated instrument designed to screen for the presence of a wide range of sleep disturbances during the preceding 3 weeks, completed by a bed partner who regularly sleeps with the subject [25]. RBD was rated as present if the bed partner reported dream enactment behavior on 3 or more occasions (score of 1). Parkinsonism was rated using the motor subscale of the Unified Parkinson s Disease Rating Scale [26], and parkinsonism was rated as present with a UPDRS motor subscale score of 10 or more [21]. P re s e n t i n g Sy m pt o m s Caregivers were interviewed by a trained research clinician regarding the presenting symptoms of dementia using a scripted list of symptoms (more than one answer was possible): reduced memory, problem solving difficulties, depression, visual hallucinations, gait problems, tremor, stiffness, tendency to fall, language problems, or other. Caregivers were also asked whether tremor or stiffness, gait problems/problems with balance or falling, visual hallucinations, delirium, or fluctuations of consciousness had ever occurred between onset and the time of assessment. The answers were further explored with detailed questioning by the clinician and recorded as present or absent. Disease duration was defined as the time from occurrence of the presenting symptom until baseline assessment. The final diagnosis was not known at the time of administering this questionnaire. Patients were classified as mildly or very mildly demented based on their median MMSE total score (23 for DLB patients and 24 for AD patients) Dopamine Transporter SPECT Imaging Dopamine transporter imaging was performed by intravenous injection of approximately 185 MBq [ 123 I]FP-CIT. Typically, SPECT images were acquired 3 h after injection [17]. Reconstructed images were analyzed visually by an experienced nuclear medicine physician (J.B.) using the criteria earlier described [18]. S t a t i s t i c s SPSS/PASW statistics version 18 were used for all analyses and p = 0.05 was considered statistically significant. Pearson s 2 test was used for categorical variables and Student s t test or the Mann- Whitney U test was used for continuous parametric or nonparametric data as appropriate. R e s u l t s The study group comprised 170 subjects: 61 patients with probable DLB and 109 with probable AD. The demographics and clinical characteristics at diagnosis are shown in table 1. The presenting symptoms in DLB and AD are shown in table 2. The most commonly reported presenting symptom in the DLB group was memory impairment (57%), followed by visual hallucinations (44%), depression (34%), problem solving difficulties (33%), gait problems (28%), and tremor and stiffness (25%) ( table 2 ). This distribution differed from that in the AD group, where 99% reported impaired memory as the first symptom, followed by problem solving difficulties (28%) and depression (24%); other symptoms were rare (i.e.!10%). All but three symptoms (language problems, problem solving difficulties, and depression) differed significantly between the groups at the p! level. Among the 26 DLB patients with pathological dopamine transporter imaging, the findings were similar to those of the total group; cognitive impairment (42%) and visual hallucinations (42%) were the most common pre- 204 Auning /Rongve /Fladby /Booij / Hortobágyi /Siepel /Ballard /Aarsland

4 Table 2. Presenting symptoms of DLB and AD DLB (n = 61) AD (n = 109) DLB and abnormal DAT scan (n = 26) p value 1 Memory impairment 35 (57.4) 108 (99.1) 11 (42.3) Visual hallucinations 27 (44.3) 3 (2.8) 11 (42.3) Depression 21 (34.4 ) 26 (23.9) 10 (38.4) Problem-solving difficulties 20 (32.8) 31 (28.4) 8 (30.8) Gait problems 17 (27.9) 9 (8.3) 7 (26.9) Tremor and/or stiffness 15 (24.6) 4 (3.7) 10 (38.4) Language problems 10 (16.4) 19 (17.4) 2 (7.7) Tendency to fall 8 (13.1) 4 (3.7) 4 (15.4) V alues are presented as patient numbers (%). 1 DLB (n = 61) and AD (n = 109) compared. More than one symptom can be reported. Table 3. Symptoms prior to the dementia stage DLB (n = 61) AD (n = 109) p value Visual hallucinations 47 (77.0) 7 (6.4) Gait problems, problems with balance or falling 40 (65.6) 21 (19.3) Tremor or stiffness 36 (59.0) 11 (10.1) Delirium/fluctuations of consciousness 26 (42.6) 15 (13.8) V alues are presented as patient numbers (%). senting symptoms, followed by depression (38%) and tremor/stiffness (38%). We also analyzed the distribution of presenting symptoms in male and female DLB patients separately, and there were no differences between genders (data not shown). Table 3 shows the frequency of core features which occurred prior to diagnosis. In DLB, visual hallucinations occurred in 77% of the patients, gait problems/problems with balance or falling in 66%, tremor/stiffness in 59%, and delirium/attentional fluctuations in 43%. In contrast, and as expected, such symptoms were much less common in AD (all p! ). Upon assessment, parkinsonism was present in 64% of DLB patients, visual hallucinations in 59%, cognitive fluctuations in 43%, and RBD in 39%. The distribution of symptoms between AD and DLB did not differ significantly when patients with mild or very mild dementia were analyzed separately, but cognitive fluctuations were numerically more common in the mildly demented (50.0%) compared to very mildly (33.3%) demented (p = 0.191) DLB patients (data not shown). Discussion Caregivers reported memory impairment (57%), visual hallucinations (44%), depression (34%), and problem solving difficulties (33%) as the most common presenting symptoms in DLB. Among the core features, visual hallucinations (77%) were the most common symptom prior to the first assessment, followed by parkinsonism ( 60%) and delirium/fluctuating cognition (43%). Very few previous studies have attempted to determine the presenting symptoms of a relatively large group of DLB patients. In one autopsy-based study exploring the symptom profile upon initial assessment at a memory clinic, visual hallucinations were the best positive predictor and absence of visuospatial impairment the strongest negative predictor of a diagnosis of DLB versus AD [27]. This is consistent with our finding that visual hallucinations are one of the most common presenting symptoms in DLB but not in AD. Case studies of prospectively followed subjects have shown that PAF and RBD may be presenting symptoms of DLB as well, whereas fluctuating cognition seems to occur late in the disease process of DLB [8]. This is con- Early and Presenting Symptoms of DLB 205

5 sistent with our finding that fluctuating cognition was less common in the earliest disease stages of DLB. Fluctuating cognition may be difficult to detect and was the least common core feature at the examination. Inte r p re t at ion The findings provide some indications regarding the initial brain changes in DLB. The progression of brain changes in DLB is not known in detail, nor are the brain changes underlying the core features well understood. The exception is parkinsonism which is mainly related to nigrostriatal pathologies [28], and there are some indications that visual hallucinations are related to temporal lobe Lewy bodies and cholinergic changes [29, 30]. Thus, the observed sequence of symptoms, with cognitive impairment and visual hallucinations occurring before parkinsonism, suggests that cortical or forebrain changes may induce clinical signs earlier than degenerative changes of the brainstem. Thus, a top-down clinical progression rather than the bottom-up pathological progression as suggested by Braak et al. [31] for PD may be a more common pattern in DLB, at least to explain the clinical progression, which is consistent with the results of previous autopsy studies [32]. Indeed, it is of interest that 26 out of 33 DLB cases (79%) had a loss of striatal dopamine transporters, indicating degeneration of nigrostriatal cells, although a lower percentage (64% had parkinsonian signs. This finding is in agreement with the findings of previous studies in DLB, which also reported cases with loss of striatal dopamine transporters and no parkinsonism [7]. Finally, also in preclinical cases of PD significant loss of dopamine transporters can be detected [33]. However, there are several potential alternative causes for symptoms such as gait problems and stiffness in the elderly, including musculoskeletal problems. Tremor, on the other hand, is always seen as pathological [34]. L i m i t a t i o n s The main limitation of this study is the retrospective nature of eliciting presenting symptoms. Thus, the carers responses may be subject to recall bias and influenced by clinical symptoms at the time of assessment. However, given the wide range of potential presenting symptoms, conducting a prospective study would require huge resources. Memory was the most common presenting symptom in DLB, although a nonmemory cognitive profile is typical in DLB. However, distinguishing between different cognitive symptoms may be difficult. For example, in one study of 15 patients with PDD, memory impairment was reported as the first complaint in 67% of the patients, in contrast to objective measurement suggesting that attention, executive, and visuospatial impairment is more common [35]. Similarly, previous studies of PD patients have shown that, in the presence of parkinsonism, carers may either over- or underreport cognitive impairment [36]. On the other hand a recent study suggests that caregivers are sensitive in detecting early cognitive deficits not ordinarily found upon routine clinical assessment [37]. In this study caregiver ratings of memory impairment correlated not only with memory and learning deficits but also with poorer performance on domains such as executive functioning, language, and psychomotor speed, suggesting that carers have difficulty distinguishing memory impairment from other cognitive deficits. We used a semistructured method to explore the presenting symptoms, identifying problems from a checklist but allowing for clinical clarification when indicated. The sensitivity and specificity of this method have not been assessed, and thus the accuracy of this method is unknown. Furthermore, the list is not exhaustive, and symptoms such as fluctuating cognition, getting lost, and apathy were not offered as an option for a presenting symptom. This might have influenced the findings, although caregivers own suggestions were an alternative if needed. Another potential effect of retrospectively assessing presenting symptoms is that since the presenting symptoms were known to the clinician during the assessment this might have lead to increased sensitivity to detect such symptoms during the assessment and thus diagnose DLB, i.e. risk of circularity. The diagnosis of AD and DLB was based on clinical assessments, and thus some misclassification may occur. However, previous versions of the clinical consensus criteria had a very high specificity. In addition, patients were followed longitudinally, and standardized instruments employing empirically based cutoff values were used. Finally, dopamine transporter scans were available for a subgroup of the DLB patients, and the clinical diagnosis was pathologically confirmed in the five patients with a pathological diagnosis. Thus, we believe that the clinical diagnoses of AD and DLB are accurate. Participants were selected from psychiatric, neurology, and geriatric clinics. Consequently, patients developing DLB and presenting at other clinics, or those who were not referred, were not included. Thus, we might have missed early DLB cases with a clinical profile character- 206 Auning /Rongve /Fladby /Booij / Hortobágyi /Siepel /Ballard /Aarsland

6 ized by RBD, who might present to sleep clinics and possibly not be referred further. However, with only one sleep center in the region, this number is expected to be small. Since we selectively recruited DLB patients during the last stage of the recruitment phase, the distribution of AD versus DLB is not representative of the mild dementia population. However, since we aimed to recruit from several clinical sources, including psychiatry, geriatric medicine, and neurology, we think that the DLB cohort is representative of a referral cohort of DLB. Implications The present findings have potential clinical implications. First, since memory impairment is among the most common presenting symptoms, DLB should be considered as a diagnostic option also in subjects with early memory complaints. Visual hallucinations were the second most common presenting symptom and, if occurring in an elderly person, may signal the development of a fullblown DLB syndrome; thus such patients should be followed carefully. To conclude, cognitive impairment and visual hallucinations were the most common presenting symptom in DLB. Future studies exploring the initial symptoms of DLB should prospectively describe the clinical development in subjects recruited from a range of different sources, such as sleep centers and psychiatric, movement, and autonomic disorder clinics in addition to memory clinics. Disclosure Statement E.A., A.R., T.F., and F.J.S. report no disclosures. J.B. is a consultant at GE Healthcare. T.H. serves on the editorial boards of Acta Neuropathologica, Central European Journal of Medicine, and Frontiers in Neurodegeneration, and receives honoraria from the Italian ALS Research Foundation (AriSLA) as an International Scientific Committee member. C.B. has received consultancy fees from Novartis, Lundbeck, Eisai, Acadia, and Bristol-Myers Squibb; honoraria from Lundbeck, Novartis, Eisai, and Acadia; payment for manuscript preparation from Bristol-Myers Squibb, and travel and accommodation expenses from Lundbeck, Acadia, Novartis, Eisai, and Bristol- Myers Squibb. Clive Ballard s institution has received grants from Lundbeck and Acadia and grants from Lundbeck, Novartis, Eisai, and Acadia. D.A. serves on scientific advisory boards for Lundbeck, Inc., and Merck Serono; has received funding for travel and speaker honoraria from Lundbeck, Inc., Novartis, GE Healthcare, and GlaxoSmithKline; serves on the editorial boards of International Psychogeriatrics, Movement Disorders, and the Journal of Neurology, Neurosurgery, and Psychiatry, and receives research support from Lundbeck, Inc., and Merck Serono. 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