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Journal of Alzheimer’s Disease 39 (2014) 883–889 DOI 10.3233/JAD-131601 IOS Press
Dementia among Elderly in Shanghai Suburb: A Rural Community Survey Qi Chenga,b,∗ , Hong-Xian Suna,b , Fu-Lin Yec , Gang Wanga , Hua-Wei Lingd , Sheng-Di Chena,∗ and Guo-Xin Jiange a Department
of Neurology, Ruijin Hospital affiliated with the School of Medicine, Shanghai Jiao Tong University, Shanghai, China b School of Public Health, Shanghai Jiao Tong University, Shanghai, China c Sheshan Town Community Health Service Center in Shanghai, Shanghai, China d Department of Radiology, Ruijin Hospital affiliated with the School of Medicine, Shanghai Jiao Tong University, Shanghai, China e Department of Public Health Sciences, Karolinska Institute, Stockholm, Sweden
Accepted 22 October 2013
Abstract. The number of elderly in the world is increasing rapidly, especially in China. The prevalence of dementia among elderly was investigated in a community of Sheshan town, located in the Southwest suburb of Shanghai, China. Face-to-face interviews were conducted to collect relevant information with prepared questionnaires. The Chinese version of the Mini-Mental Status Examination was used to screen subjects with cognitive impairment (CI). Physical examinations and neuropsychological assessments were carried out. Dementia and its major subtypes, Alzheimer’s disease (AD) and vascular dementia (VaD), were diagnosed by senior neurologists according to relevant diagnostic criteria. In addition, magnetic resonance imaging and EEG (with P300) were performed for a number of cases with AD or VaD. There were 1,472 participants (666 males and 806 females) aged 60 years and over in the study. A total of 167 subjects with CI were screened. Among them, dementia was recognized in 79 cases with a prevalence of 5.37% (95% confidence intervals: 4.22%–6.52%). The diagnosis of AD was made for 53 cases (16 males and 37 females) with a prevalence of 3.60% (95% confidence intervals: 2.65%–4.55%), and VaD for 21 cases (5 males and 16 females) with a prevalence of 1.43% (95% confidence intervals: 0.82%–2.03%); while the ratio of AD to VaD was 2.52. The prevalence rates of dementia among elderly from our study are higher than that previously reported from China, but in line with that reported from most world regions. A nationwide survey and surveillance system on the prevalence of dementia is recommended. Keywords: Alzheimer’s disease, dementia, prevalence, vascular dementia
INTRODUCTION
∗ Correspondence
to: Qi Cheng, School of Public Health, Shanghai Jiao Tong University, 227 Chong Qing Nan Road, Shanghai 200025, China. Tel./Fax: +86 21 53061167; E-mail: [email protected]; Sheng-Di Chen, Department of Neurology, Ruijin Hospital affiliated with the School of Medicine, Shanghai Jiao Tong University, 197 Ruijin No. 2 Road, Shanghai 200025, China. Tel.: +86 21 64370045; E-mail: chen [email protected].
The number and the proportion of elderly in the world are increasing rapidly, especially in China. Dementia is one of the main causes of disability and decreased quality of life. Patients suffering from dementia have different cognitive, behavioral, and neuropsychiatric symptoms. It was estimated that there were around 24 million people with dementia in the world in 2001 and the majority of them were
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considered to have Alzheimer’s disease (AD) [1]. Recently, a new estimation was suggested that 35.6 million people lived with dementia worldwide in 2010, with the number expected to almost double every 20 years, to 65.7 million in 2030 and 115.4 million in 2050 [2]. Prevalence rates of dementia and AD or other main subtypes of dementia are available from a number of countries. In the United States, 5.4 million people were estimated to have AD currently, and AD is the sixth leading cause of death [3]. A collaborative study with 11 population-based cohorts including 2,346 cases of dementia from Europe reported an agestandardized prevalence of 6.4% for dementia [4.4% for AD and 1.6% for (vascular dementia (VaD)] among people aged 65 years and over [4]. In 1997, a crosssectional prevalence survey in four cities in China reported a prevalence of 3.5% for AD and 1.1% for VaD among people aged 65 years and over [5]. In the current study, we describe results from a community survey on dementia and its major subtypes, AD and VaD, among elderly in Shanghai suburb. MATERIALS AND METHODS Study population Subjects in the study were from a community of Sheshan town in Songjiang district, located in the Southwest suburb of Shanghai. All residents aged 60 years and over with permanent residence in the town were eligible to participate in our study. There are 11 towns in Songjiang district. According to the latest national census in 2010, the number of people with permanent residence in the district was 575,185 in total, and the proportion of people aged 60 years and over was 20.8%. The residents in the district mainly engage in vegetable planting, foodstuff planting, and breeding. Screening for cognitive impairment The Chinese version of the Mini-Mental Status Examination (C-MMSE) was used to screen subjects with cognitive impairment (CI) in our study participants. According to the educational level of the respondents, cutoff points of C-MMSE were: 17/18 for those without formal education, 20/21 for those with 1–6 years of education (primary school), and 24/25 for those with more than 6 years of education (middle school or higher). Subjects with the C-MMSE score lower than the cutoff points were considered as having CI [6].
Assessment of dementia All-cause dementia was diagnosed according to the DSM-IV criteria [7]. A dementia patient manifests symptoms of CI detected and diagnosed through a combination of medical history and an objective cognitive assessment. Cognitive deficits present a decline from previous functioning and cause significant impairment in social or occupational functioning, and the symptoms are not explained by delirium or major psychiatric disorders. Clinical subtypes of dementia The diagnostic criteria for AD, revised by the National Institute on Aging and the Alzheimer’s Association (NIA-AA) in 2011 [8], were followed in our study, and the general criteria for dementia had to also be met. Mainly, the NIA-AA diagnostic criteria require: insidious onset, clear-cut history of worsening of cognition by report or observation, and the initial and most prominent cognitive deficits in amnestic presentation, language presentation, visuospatial presentation, and executive dysfunction. In addition, there is no evidence from the history, physical examination, or special investigations for any other possible cause of dementia (e.g., cerebrovascular disease, Parkinson’s disease, Huntington’s disease, normal pressure hydrocephalus), a systemic disorder (e.g., hypothyroidism, vitamin B12 or folic acid deficiency, hypercalcaemia), or alcohol- or drug-abuse. The diagnosis of VaD was made according to the National Institute of Neurological Disorders and Stroke/the Association Internationale pour la Recherche et l’Enseignement en Neurosciences (NINDS-AIREN) criteria [9]. The clinical diagnosis of probable VaD mainly includes dementia defined by cognitive decline from a previously higher level of functioning and manifested by impairment of memory and of two or more cognitive domains (orientation, attention, language, visuospatial functions, executive functions, motor control, and praxis) and cerebrovascular disease, defined by the presence of focal signs on neurologic examination, and the evidence of relevant cerebrovascular diseases by brain imaging (CT or MRI). Investigation procedures The investigation was conducted in 2011. Four interviewers, who had been specifically trained and participated in our previous investigations with C-
Q. Cheng et al. / Dementia among Elderly in Shanghai Suburb
MMSE [10], conducted the screening procedure and the interview with prepared questionnaires. Subjects with the C-MMSE score lower than the cutoff points according to the educational level were recognized as having CI. Subjects with CI were further examined by neurologists from the Department of Neurology, Ruijin Hospital. In addition to the results from C-MMSE, detailed medical history from the subject and a knowledgeable informant, as well as family history, were obtained. Neurological examinations and neuropsychological assessments like Activities of Daily Living (ADL) and Hachinski Ischemia Scale (HIS) were performed. The Chinese version of the Cornell Scale for Depression in Dementia (CSDD) [11] was used to assess the mood fluctuation in dementia. A preliminary diagnosis of dementia and its clinical subtypes for a number of subjects were made by neurologists, following the diagnostic criteria as aforementioned. In addition, all cases with dementia were followed up six months later, in order to confirm the diagnosis. In the meantime, MRI and EEG P300 examinations were offered free of charge to all cases with AD or VaD. Finally, all information and relevant data including detailed medical history, family history, results of neurological examinations and neuropsychological tests, as well as laboratory or brain imaging examinations were compiled for each case with a preliminary diagnosis of dementia, and scrutinized by four senior neurologists individually to validate the diagnosis of dementia and its clinical subtypes. Whenever there was a disagreement, discussions were conducted until achieving a concord. The study was approved by Ethics Committee of Ruijin Hospital, Shanghai Jiao Tong University. All eligible participants were encouraged to participate in the survey but free to decline. Informed consent was signed by participants or their legal guardian for those severely demented or inked with a thumbprint in lieu of signature for those illiterate. Statistical methods The prevalence rate of dementia or its subtypes was calculated with the number of subjects with dementia or its subtypes as the numerator, and the number of all participants in the study as the denominator. All measurement data were expressed as means (standard deviation, SD). The 2-independent-sample t test was used for continuous variables and differences between groups were determined by using Chi-square tests,
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when appropriate. All statistical analyses were performed using the Statistical Package for Social Science (SPSS). All p values were based on two-sided tests with a significance level of 0.05. RESULTS Study subjects In the Sheshan town, 2,052 residents aged 60 years and over were eligible to participate in the study. Among them, 1,472 subjects (71.7%) completed the interview and C-MMSE (Fig. 1). The mean age was 69.67 (SD: 7.11) years for all participants, 69.66 (SD: 6.80) years for men, and 69.67 (SD: 7.36) years for women. People unwilling or unable to complete the survey due to hearing impairment, speech problems, or refusal to cooperate were excluded from the study. The majority of participants were female (54.80%), married (89.40%), farmer (93.34%), and without formal education (56.3%). Compared to those who were eligible but did not participate in the study, women were overrepresented as study participants (p < 0.001) because more men did not participate due to different reasons like the lower compliance of participation in men than women. In addition, the participants were relatively older than the non-participants (p < 0.001) because fewer younger people would like to join our study. Subjects with CI There were 167 subjects with C-MMSE scores lower than the cutoff points according to the educational level, and the proportion of subjects with CI in the participants was 11.35% (9.61% for males and 12.78% for females). There were more female subjects with CI than males (p = 0.056) (Table 1). Prevalence of dementia and its subtypes Finally, 79 cases were diagnosed as dementia, with a prevalence of 5.37% (95% confidence intervals: 4.22%–6.52%), 3.30% (95% confidence intervals: 1.95%–4.66%) for males, and 7.07% (95% confidence intervals: 5.30%–8.84%) for females (Table 2), significantly higher in females (p = 0.001). Among the 79 cases with dementia, 53 cases were diagnosed as AD, with a prevalence of 3.60% (4.59% for females and 2.40% for males); 21 cases were classified as VaD, with a prevalence of 1.43% (1.99% for females and 0.75% for males); and the other five cases
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Fig. 1. Results of investigation for dementia and its subtypes. C-MMSE, Chinese version of the Mini-Mental Status Examination; AD, Alzheimer’s disease; VaD, vascular dementia; OD, other types of dementia. Table 1 Subjects with cognitive impairment (CI) by gender, age group, and education level Age group (years)
Without formal education (6 years) 60–69 70–79 80+ Subtotal Total
Male
Female
All
No. of subjects with CI (%)
No. of participants
No. of subjects with CI (%)
No. of participants
No. of subjects with CI (%)
No. of participants
4 (5.1) 14 (15.4) 7 (17.1) 25 (11.9)
78 91 41 210
12 (4.3) 43 (17.5) 37 (39.4) 92 (14.9)
278 246 94 618
16 (4.5) 57 (16.9) 44 (32.6) 117 (14.1)
356 337 135 828
8 (4.3) 11 (13.1) 6 (26.1) 25 (8.5)
186 84 23 293
8 (5.8) 1 (5.6) 0 (0.0) 9 (5.7)
137 18 2 157
16 (5.0) 12 (11.8) 6 (24.0) 34 (7.6)
323 102 25 450
7 (5.8) 5 (13.9) 2 (33.3) 14 (8.6) 64 (9.6)
121 36 6 163 666
2 (7.7) 0 (0.0) 0 (0.0) 2 (6.5) 103 (12.8)
26 5 0 31 806
9 (6.1) 5 (12.2) 2 (33.3) 16 (8.2) 167 (11.3)
147 41 6 194 1472
(0.34%) with extrapyramidal symptoms were considered as secondary dementia and termed as other types of dementia (OD). Prevalence rates of both AD and VaD were higher in females than in males and increasing with age, while the ratio of AD to VaD was 2.52. In total, 34 (45.9%) cases were examined with MRI and EEG P300, based on the feasibility and accep-
tance of participants. Among them, 26 cases were diagnosed as AD and the other 8 cases as VaD, before the examinations. In general, results from the examinations corresponded to and supported the clinical diagnoses, while for three cases, the preliminary diagnosis of AD was revised to VaD based on the results from MRI. Examples of MRI images for a case with
Q. Cheng et al. / Dementia among Elderly in Shanghai Suburb Table 2 Number and prevalence (%) of dementia and its subtypes by gender and age group Age group Alzheimer’s disease 60–69 70–79 80+ Subtotal Vascular dementia 60–69 70–79 80+ Subtotal Other types of dementia 60–69 70–79 80+ Subtotal All dementia 60–69 70–79 80+ Total
Male n (%)
Female n (%)
All n (%)
4 (1.04) 6 (2.84) 6 (8.57) 16 (2.40)
5 (1.13) 17 (6.32) 15 (15.63) 37 (4.59)
9 (1.09) 23 (4.79) 21 (12.65) 53 (3.60)
1 (0.26) 3 (1.42) 1 (1.43) 5 (0.75)
1 (0.23) 8 (2.97) 7 (7.29) 16 (1.99)
2 (0.24) 11 (2.29) 8 (4.82) 21(1.43)
0 (0.0) 1 (0.47) 0 (0.0) 1 (0.15)
1 (1.59) 2 (0.74) 1 (1.04) 4 (0.50)
1 (0.12) 3 (0.63) 1 (0.60) 5 (0.34)
5 (1.30) 10 (4.74) 7 (10.00) 22 (3.30)
7 (1.59) 27 (10.04) 23 (23.96) 57 (7.07)
12 (1.45) 37 (7.71) 30 (18.07) 79 (5.37)
AD and a case with VaD are presented in Fig. 2. The EEG examinations might be useful for excluding other diseases, but not so helpful in the differentiation of AD from VaD. DISCUSSION A population-based survey among elderly aged 60 years and over was conducted in Sheshan town located in the Southwest suburb of Shanghai with a response rate of over 70%. The majority of the participants in our study were low-educated farmers, and there were more women than men. Generalization of our results should be cautious due to the characteristics of our study participants. For example, a low-educated population may tend to have a relatively higher prevalence of dementia, compared to a high-educated population. In addition, VaD usually occurs more frequently in men [12], which may be determined by other relevant risk factors. We used C-MMSE to identify subjects with CI, which was initially modified by Katzman et al. [13]. The C-MMSE takes around 15–20 minutes to administer, covering various areas of cognitive domains (e.g., orientation, memory, language, and visual construction), and has been proven to be effective in assessing those with different educational backgrounds including illiteracy [13, 14]. According to our previous experience [10], it is appropriate to adjust the cut-
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off points of C-MMSE for the criteria of CI with the educational level, particularly in a low-educated study population. The MMSE is widely used in the screen phase in many epidemiological studies on dementia in the world and is considered a reliable tool to screen for moderate and severe dementia [15]. In the recent decades, a number of studies from China reported prevalence rates of dementia and its major subtypes. A meta-analysis [16] summarized results from 48 surveys on dementia prevalence in China during the period of 1980–2010 and made a pooled prevalence of 3.0% (95% confidence intervals: 2.4%–3.9%) for dementia in the population aged 60 years and over, 1.9% (95% confidence intervals: 1.4%–2.4%) for AD and 0.9% (95% confidence intervals: 0.6%–1.1%) for VaD. Compared to the results from these previous reports in China, prevalence rates of dementia as well as its major subtypes from our study are higher. The difference may be explained in part by the age difference of study participants. Although the mean age for all participants was not described, the pooled prevalence of dementia for participants aged 65 years and over was reported as 6.0% in that meta-analysis [16]. While the mean age of our study participants was 69.67 years. On the other hand, our results are in line with that reported from most world regions, as disclosed by the recently published review and meta-analysis on the global prevalence of dementia, in which most of the estimated agestandardized prevalence rates of dementia were in a range between 5% and 7% for all aged 60 years and over [15]. In our results, AD accounted for around two-thirds, while VaD for one-fourth, of all dementia. The ratio of prevalence between AD and VaD was 2.52, which is almost the same as that (2.50) based on the weighted prevalence of AD and VaD for both genders, reported from the study conducted in four cities in China [5]. In the article with 2,346 cases of dementia from Europe, the ratio of prevalence between AD and VaD was 2.75 [4]. In an article from Japan [17], trends in the prevalence of AD and VaD among elderly over 20 years (1980–2000) were examined. The ratio of the prevalence of AD to VaD increased remarkably over the 20 years, which was attributed by authors to the significantly increased AD prevalence during the period. The classification of AD and VaD may be difficult sometimes, because there are no definite clinical and pathological diagnostic consensus criteria, and the high frequency of mixed pathologies in very old subjects [18, 19]. A definitive diagnosis of AD can only be made with the histopathologic examination of either biopsy
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Fig. 2. Magnetic resonance imaging images for a case with Alzheimer’s disease (AD) and a case with vascular dementia (VaD). A) Female, 78 years, AD. Bilateral hippocampal atrophy and widened parahippocampal sulcus. No significant infarcts observed at the level of the lateral ventricles with T2 W. B) Female, 80 years, VaD. No obvious hippocampal atrophy. Multiple patchy high signals indicating infarcts in the bilateral frontal lobes with T2W.
or postmortem brain tissue [20, 21]. The development of brain imaging techniques during the recent several decades has greatly improved the degree of certainty for diagnosis of dementia. Imaging examinations like CT and MRI are a great help, and 45.9% of all cases with AD or VaD in our study were examined with MRI, which lends confidence about the validity of our classification for cases with AD or VaD. While the diagnosis for dementia is basically clinical, MRI examination is important for the differentiation between AD and VaD. The predominance of females in dementia is observed from most epidemiological surveys. In the meantime, the prevalence rates of dementia and its major subtypes, AD and VaD, are increasing with age [1–5, 16]. Both are valid in the current study. Aging is increasing, especially in China, where the one-child family policy has been effective for more than 30 years. Therefore, it can be expected
that the number of prevalent cases with dementia will increase rapidly in China, which requires a better planning and caring system. In order to wellprepare for and overcome the increasing challenge in China, a nationwide survey and surveillance system on the prevalence of dementia is recommended. As having been commented, such a nationwide survey on the prevalence of dementia is still lacking in the world, particularly in developing countries [15, 22, 23]. In conclusion, the prevalence rates of dementia among elderly from our study are higher than that previously reported from China, but in line with that reported from most world regions. Dementia and its major subtypes, AD and VaD, are more prevalent in women and increasing with age. A nationwide survey and surveillance system on the prevalence of dementia is recommended.
Q. Cheng et al. / Dementia among Elderly in Shanghai Suburb
ACKNOWLEDGMENTS This study was supported by funds from Natural Science Foundation of China (81070958 & 81371218), Shanghai Municipal Health Bureau Key disciplines (12GWZX0101), and Shanghai Science and Technology Commission (07DJ14005). We appreciate the kind support from caregivers of the Community Health Service Centre in Sheshan town and all neurologists, who were involved in the study, at the Department of Neurology, Ruijin Hospital, School of Medicine, Shanghai Jiao Tong University. Authors’ disclosures available online (http://www.jalz.com/disclosures/view.php?id=2000). REFERENCES [1]
[2]
[3]
[4]
[5]
[6]
[7]
[8]
Ferri CP, Prince M, Brayne C, Brodaty H, Fratiglioni L, Ganguli M, Hall K, Hasegawa K, Hendrie H, Huang Y, Jorm A, Mathers C, Menezes PR, Rimmer E, Scazufca M, Alzheimer’s Disease International (2005) Global prevalence of dementia: A Delphi consensus study. Lancet 366, 2112-2117. Prince M, Bryce R, Albanese E, Wimo A, Ribeiro W, Ferri CP (2013) The global prevalence of dementia: A systematic review and metaanalysis. Alzheimers Dement 9, 63-75. Thies W, Bleiler L, Alzheimer’s Association (2013) Alzheimer’s disease facts and figures. Alzheimers Dement 9, 208-245. Lobo A, Launer LJ, Fratiglioni L, Andersen K, Di Carlo A, Breteler MM, Copeland JR, Dartigues JF, Jagger C, MartinezLage J, Soininen H, Hofman A (2000) Prevalence of dementia and major subtypes in Europe: A collaborative study of population-based cohorts. Neurologic Diseases in the Elderly Research Group. Neurology 54, S4-S9. Zhang ZX, Zahner GE, Rom´an GC, Liu J, Hong Z, Qu QM, Liu XH, Zhang XJ, Zhou B, Wu CB, Tang MN, Hong X, Li H (2005) Dementia subtypes in China: Prevalence in Beijing, Xian, Shanghai, and Chengdu. Arch Neurol 62, 447-453. Cui GH, Yao YH, Xu RF, Tang HD, Jiang GX, Wang Y, Wang G, Chen SD, Cheng Q (2011) Cognitive impairment using education-based cutoff points for CMMSE scores in elderly Chinese people of agricultural and rural Shanghai China. Acta Neurol Scand 124, 361-367. American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders, 4th ed., text revised (DSM-IV-TR). American Psychiatric Association, Washington, DC. McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR Jr, Kawas CH, Klunk WE, Koroshetz WJ, Manly JJ, Mayeux R, Mohs RC, Morris JC, Rossor MN, Scheltens P, Carrillo MC, Thies B, Weintraub S, Phelps CH (2011) The diagnosis of dementia due to Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 7, 263-269.
[9]
[10]
[11]
[12] [13]
[14]
[15]
[16]
[17]
[18] [19] [20] [21] [22]
[23]
889
Rom´an GC, Tatemichi TK, Erkinjuntti T, Cummings JL, Masdeu JC, Garcia JH, Amaducci L, Orgogozo JM, Brun A, Hofman A, Moody DM, O’Brien MD, Yamaguchi T, Grafman J, Drayer BP, Bennett DA, Fisher M, Ogata J, Kokmen E, Bermejo F, Wolf PA, Gorelick PB, Bick KL, Pajeau AK, Bell MA, DeCarli C, Culebras A, Korczyn AD, Bogousslavsky J, Hartmann A, Scheinberg P (1993) Vascular dementia: Diagnostic criteria for research studies. Report of the NINDSAIREN International Workshop. Neurology 43, 250-260. Yao YH, Xu RF, Tang HD, Jiang GX, Wang Y, Wang G, Chen SD, Cheng Q (2010) Cognitive impairment and associated factors among the elderly in the Shanghai suburb: Findings from a low-education population. Neuroepidemiology 34, 245-252. Alexopoulos GS, Abrams RC, Young RC, Shamoian CA (1988) Cornell scale for depression in dementia. Biol Psychiatry 23, 271-284. Azad NA, Al Bugami M, Loy-English I (2007) Gender differences in dementia risk factors. Gend Med 4, 120-129. Katzman R, Zhang MY, Ouang-Ya-Qu, Wang ZY, Liu WT, Yu E, Wong SC, Salmon DP, Grant I (1988) A Chinese version of the Mini-Mental State Examination; impact of illiteracy in a Shanghai dementia survey. J Clin Epidemiol 41, 971-978. Zhang MY, Katzman R, Salmon D, Jin H, Cai GJ, Wang ZY, Qu GY, Grant I, Yu E, Levy P, Klauber MR, Liu WT (1990) The prevalence of dementia and Alzheimer’s disease in Shanghai, China: Impact of age, gender, and education. Ann Neurol 27, 428-437. Misiak B, Cialkowska-Kuzminska M, Frydecka D, Chladzinska-Kiejna S, Kiejna A (2013) European studies on the prevalence of dementia in the elderly: Time for a step towards a methodological consensus. Int J Geriatr Psychiatry 28, 1211-1221. Zhang Y, Xu Y, Nie H, Lei T, Wu Y, Zhang L, Zhang M (2012) Prevalence of dementia and major dementia subtypes in the Chinese populations: A meta-analysis of dementia prevalence surveys, 1980-2010. J Clin Neurosci 19, 1333-1337. Dodge HH, Buracchio TJ, Fisher GG, Kiyohara Y, Meguro K, Tanizaki Y, Kaye JA (2012) Trends in the prevalence of dementia in Japan. Int J Alzheimers Dis 2012, 956354. Jellinger KA, Attems J (2010) Is there pure vascular dementia in old age? J Neurol Sci 299, 150-154. Cumming TB, Brodtmann A (2011) Can stroke cause neurodegenerative dementia? Int J Stroke 6, 416-424. Ballard C, Gauthier S, Corbett A, Brayne C, Aarsland D, Jones E (2011) Alzheimer’s disease. Lancet 377, 1019-1031. Mawanda F, Wallace R (2013) Can infections cause Alzheimer’s disease? Epidemiol Rev 35, 161-180. Kalaria RN, Maestre GE, Arizaga R, Friedland RP, Galasko D, Hall K, Luchsinger JA, Ogunniyi A, Perry EK, Potocnik F, Prince M, Stewart R, Wimo A, Zhang ZX, Antuono P, World Federation of Neurology Dementia Research, Group (2008) Alzheimer’s disease and vascular dementia in developing countries: Prevalence, management, and risk factors. Lancet Neurol 7, 812-826. Venketasubramanian N, Sahadevan S, Kua EH, Chen CP, Ng TP (2010) Interethnic differences in dementia epidemiology: Global and Asia-Pacific perspectives. Dement Geriatr Cogn Disord 30, 492-498.
Journal of Alzheimer’s Disease 39 (2014) 883–889 DOI 10.3233/JAD-131601 IOS Press
Dementia among Elderly in Shanghai Suburb: A Rural Community Survey Qi Chenga,b,∗ , Hong-Xian Suna,b , Fu-Lin Yec , Gang Wanga , Hua-Wei Lingd , Sheng-Di Chena,∗ and Guo-Xin Jiange a Department
of Neurology, Ruijin Hospital affiliated with the School of Medicine, Shanghai Jiao Tong University, Shanghai, China b School of Public Health, Shanghai Jiao Tong University, Shanghai, China c Sheshan Town Community Health Service Center in Shanghai, Shanghai, China d Department of Radiology, Ruijin Hospital affiliated with the School of Medicine, Shanghai Jiao Tong University, Shanghai, China e Department of Public Health Sciences, Karolinska Institute, Stockholm, Sweden
Accepted 22 October 2013
Abstract. The number of elderly in the world is increasing rapidly, especially in China. The prevalence of dementia among elderly was investigated in a community of Sheshan town, located in the Southwest suburb of Shanghai, China. Face-to-face interviews were conducted to collect relevant information with prepared questionnaires. The Chinese version of the Mini-Mental Status Examination was used to screen subjects with cognitive impairment (CI). Physical examinations and neuropsychological assessments were carried out. Dementia and its major subtypes, Alzheimer’s disease (AD) and vascular dementia (VaD), were diagnosed by senior neurologists according to relevant diagnostic criteria. In addition, magnetic resonance imaging and EEG (with P300) were performed for a number of cases with AD or VaD. There were 1,472 participants (666 males and 806 females) aged 60 years and over in the study. A total of 167 subjects with CI were screened. Among them, dementia was recognized in 79 cases with a prevalence of 5.37% (95% confidence intervals: 4.22%–6.52%). The diagnosis of AD was made for 53 cases (16 males and 37 females) with a prevalence of 3.60% (95% confidence intervals: 2.65%–4.55%), and VaD for 21 cases (5 males and 16 females) with a prevalence of 1.43% (95% confidence intervals: 0.82%–2.03%); while the ratio of AD to VaD was 2.52. The prevalence rates of dementia among elderly from our study are higher than that previously reported from China, but in line with that reported from most world regions. A nationwide survey and surveillance system on the prevalence of dementia is recommended. Keywords: Alzheimer’s disease, dementia, prevalence, vascular dementia
INTRODUCTION
∗ Correspondence
to: Qi Cheng, School of Public Health, Shanghai Jiao Tong University, 227 Chong Qing Nan Road, Shanghai 200025, China. Tel./Fax: +86 21 53061167; E-mail: [email protected]; Sheng-Di Chen, Department of Neurology, Ruijin Hospital affiliated with the School of Medicine, Shanghai Jiao Tong University, 197 Ruijin No. 2 Road, Shanghai 200025, China. Tel.: +86 21 64370045; E-mail: chen [email protected].
The number and the proportion of elderly in the world are increasing rapidly, especially in China. Dementia is one of the main causes of disability and decreased quality of life. Patients suffering from dementia have different cognitive, behavioral, and neuropsychiatric symptoms. It was estimated that there were around 24 million people with dementia in the world in 2001 and the majority of them were
ISSN 1387-2877/14/$27.50 © 2014 – IOS Press and the authors. All rights reserved
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considered to have Alzheimer’s disease (AD) [1]. Recently, a new estimation was suggested that 35.6 million people lived with dementia worldwide in 2010, with the number expected to almost double every 20 years, to 65.7 million in 2030 and 115.4 million in 2050 [2]. Prevalence rates of dementia and AD or other main subtypes of dementia are available from a number of countries. In the United States, 5.4 million people were estimated to have AD currently, and AD is the sixth leading cause of death [3]. A collaborative study with 11 population-based cohorts including 2,346 cases of dementia from Europe reported an agestandardized prevalence of 6.4% for dementia [4.4% for AD and 1.6% for (vascular dementia (VaD)] among people aged 65 years and over [4]. In 1997, a crosssectional prevalence survey in four cities in China reported a prevalence of 3.5% for AD and 1.1% for VaD among people aged 65 years and over [5]. In the current study, we describe results from a community survey on dementia and its major subtypes, AD and VaD, among elderly in Shanghai suburb. MATERIALS AND METHODS Study population Subjects in the study were from a community of Sheshan town in Songjiang district, located in the Southwest suburb of Shanghai. All residents aged 60 years and over with permanent residence in the town were eligible to participate in our study. There are 11 towns in Songjiang district. According to the latest national census in 2010, the number of people with permanent residence in the district was 575,185 in total, and the proportion of people aged 60 years and over was 20.8%. The residents in the district mainly engage in vegetable planting, foodstuff planting, and breeding. Screening for cognitive impairment The Chinese version of the Mini-Mental Status Examination (C-MMSE) was used to screen subjects with cognitive impairment (CI) in our study participants. According to the educational level of the respondents, cutoff points of C-MMSE were: 17/18 for those without formal education, 20/21 for those with 1–6 years of education (primary school), and 24/25 for those with more than 6 years of education (middle school or higher). Subjects with the C-MMSE score lower than the cutoff points were considered as having CI [6].
Assessment of dementia All-cause dementia was diagnosed according to the DSM-IV criteria [7]. A dementia patient manifests symptoms of CI detected and diagnosed through a combination of medical history and an objective cognitive assessment. Cognitive deficits present a decline from previous functioning and cause significant impairment in social or occupational functioning, and the symptoms are not explained by delirium or major psychiatric disorders. Clinical subtypes of dementia The diagnostic criteria for AD, revised by the National Institute on Aging and the Alzheimer’s Association (NIA-AA) in 2011 [8], were followed in our study, and the general criteria for dementia had to also be met. Mainly, the NIA-AA diagnostic criteria require: insidious onset, clear-cut history of worsening of cognition by report or observation, and the initial and most prominent cognitive deficits in amnestic presentation, language presentation, visuospatial presentation, and executive dysfunction. In addition, there is no evidence from the history, physical examination, or special investigations for any other possible cause of dementia (e.g., cerebrovascular disease, Parkinson’s disease, Huntington’s disease, normal pressure hydrocephalus), a systemic disorder (e.g., hypothyroidism, vitamin B12 or folic acid deficiency, hypercalcaemia), or alcohol- or drug-abuse. The diagnosis of VaD was made according to the National Institute of Neurological Disorders and Stroke/the Association Internationale pour la Recherche et l’Enseignement en Neurosciences (NINDS-AIREN) criteria [9]. The clinical diagnosis of probable VaD mainly includes dementia defined by cognitive decline from a previously higher level of functioning and manifested by impairment of memory and of two or more cognitive domains (orientation, attention, language, visuospatial functions, executive functions, motor control, and praxis) and cerebrovascular disease, defined by the presence of focal signs on neurologic examination, and the evidence of relevant cerebrovascular diseases by brain imaging (CT or MRI). Investigation procedures The investigation was conducted in 2011. Four interviewers, who had been specifically trained and participated in our previous investigations with C-
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MMSE [10], conducted the screening procedure and the interview with prepared questionnaires. Subjects with the C-MMSE score lower than the cutoff points according to the educational level were recognized as having CI. Subjects with CI were further examined by neurologists from the Department of Neurology, Ruijin Hospital. In addition to the results from C-MMSE, detailed medical history from the subject and a knowledgeable informant, as well as family history, were obtained. Neurological examinations and neuropsychological assessments like Activities of Daily Living (ADL) and Hachinski Ischemia Scale (HIS) were performed. The Chinese version of the Cornell Scale for Depression in Dementia (CSDD) [11] was used to assess the mood fluctuation in dementia. A preliminary diagnosis of dementia and its clinical subtypes for a number of subjects were made by neurologists, following the diagnostic criteria as aforementioned. In addition, all cases with dementia were followed up six months later, in order to confirm the diagnosis. In the meantime, MRI and EEG P300 examinations were offered free of charge to all cases with AD or VaD. Finally, all information and relevant data including detailed medical history, family history, results of neurological examinations and neuropsychological tests, as well as laboratory or brain imaging examinations were compiled for each case with a preliminary diagnosis of dementia, and scrutinized by four senior neurologists individually to validate the diagnosis of dementia and its clinical subtypes. Whenever there was a disagreement, discussions were conducted until achieving a concord. The study was approved by Ethics Committee of Ruijin Hospital, Shanghai Jiao Tong University. All eligible participants were encouraged to participate in the survey but free to decline. Informed consent was signed by participants or their legal guardian for those severely demented or inked with a thumbprint in lieu of signature for those illiterate. Statistical methods The prevalence rate of dementia or its subtypes was calculated with the number of subjects with dementia or its subtypes as the numerator, and the number of all participants in the study as the denominator. All measurement data were expressed as means (standard deviation, SD). The 2-independent-sample t test was used for continuous variables and differences between groups were determined by using Chi-square tests,
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when appropriate. All statistical analyses were performed using the Statistical Package for Social Science (SPSS). All p values were based on two-sided tests with a significance level of 0.05. RESULTS Study subjects In the Sheshan town, 2,052 residents aged 60 years and over were eligible to participate in the study. Among them, 1,472 subjects (71.7%) completed the interview and C-MMSE (Fig. 1). The mean age was 69.67 (SD: 7.11) years for all participants, 69.66 (SD: 6.80) years for men, and 69.67 (SD: 7.36) years for women. People unwilling or unable to complete the survey due to hearing impairment, speech problems, or refusal to cooperate were excluded from the study. The majority of participants were female (54.80%), married (89.40%), farmer (93.34%), and without formal education (56.3%). Compared to those who were eligible but did not participate in the study, women were overrepresented as study participants (p < 0.001) because more men did not participate due to different reasons like the lower compliance of participation in men than women. In addition, the participants were relatively older than the non-participants (p < 0.001) because fewer younger people would like to join our study. Subjects with CI There were 167 subjects with C-MMSE scores lower than the cutoff points according to the educational level, and the proportion of subjects with CI in the participants was 11.35% (9.61% for males and 12.78% for females). There were more female subjects with CI than males (p = 0.056) (Table 1). Prevalence of dementia and its subtypes Finally, 79 cases were diagnosed as dementia, with a prevalence of 5.37% (95% confidence intervals: 4.22%–6.52%), 3.30% (95% confidence intervals: 1.95%–4.66%) for males, and 7.07% (95% confidence intervals: 5.30%–8.84%) for females (Table 2), significantly higher in females (p = 0.001). Among the 79 cases with dementia, 53 cases were diagnosed as AD, with a prevalence of 3.60% (4.59% for females and 2.40% for males); 21 cases were classified as VaD, with a prevalence of 1.43% (1.99% for females and 0.75% for males); and the other five cases
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Fig. 1. Results of investigation for dementia and its subtypes. C-MMSE, Chinese version of the Mini-Mental Status Examination; AD, Alzheimer’s disease; VaD, vascular dementia; OD, other types of dementia. Table 1 Subjects with cognitive impairment (CI) by gender, age group, and education level Age group (years)
Without formal education (6 years) 60–69 70–79 80+ Subtotal Total
Male
Female
All
No. of subjects with CI (%)
No. of participants
No. of subjects with CI (%)
No. of participants
No. of subjects with CI (%)
No. of participants
4 (5.1) 14 (15.4) 7 (17.1) 25 (11.9)
78 91 41 210
12 (4.3) 43 (17.5) 37 (39.4) 92 (14.9)
278 246 94 618
16 (4.5) 57 (16.9) 44 (32.6) 117 (14.1)
356 337 135 828
8 (4.3) 11 (13.1) 6 (26.1) 25 (8.5)
186 84 23 293
8 (5.8) 1 (5.6) 0 (0.0) 9 (5.7)
137 18 2 157
16 (5.0) 12 (11.8) 6 (24.0) 34 (7.6)
323 102 25 450
7 (5.8) 5 (13.9) 2 (33.3) 14 (8.6) 64 (9.6)
121 36 6 163 666
2 (7.7) 0 (0.0) 0 (0.0) 2 (6.5) 103 (12.8)
26 5 0 31 806
9 (6.1) 5 (12.2) 2 (33.3) 16 (8.2) 167 (11.3)
147 41 6 194 1472
(0.34%) with extrapyramidal symptoms were considered as secondary dementia and termed as other types of dementia (OD). Prevalence rates of both AD and VaD were higher in females than in males and increasing with age, while the ratio of AD to VaD was 2.52. In total, 34 (45.9%) cases were examined with MRI and EEG P300, based on the feasibility and accep-
tance of participants. Among them, 26 cases were diagnosed as AD and the other 8 cases as VaD, before the examinations. In general, results from the examinations corresponded to and supported the clinical diagnoses, while for three cases, the preliminary diagnosis of AD was revised to VaD based on the results from MRI. Examples of MRI images for a case with
Q. Cheng et al. / Dementia among Elderly in Shanghai Suburb Table 2 Number and prevalence (%) of dementia and its subtypes by gender and age group Age group Alzheimer’s disease 60–69 70–79 80+ Subtotal Vascular dementia 60–69 70–79 80+ Subtotal Other types of dementia 60–69 70–79 80+ Subtotal All dementia 60–69 70–79 80+ Total
Male n (%)
Female n (%)
All n (%)
4 (1.04) 6 (2.84) 6 (8.57) 16 (2.40)
5 (1.13) 17 (6.32) 15 (15.63) 37 (4.59)
9 (1.09) 23 (4.79) 21 (12.65) 53 (3.60)
1 (0.26) 3 (1.42) 1 (1.43) 5 (0.75)
1 (0.23) 8 (2.97) 7 (7.29) 16 (1.99)
2 (0.24) 11 (2.29) 8 (4.82) 21(1.43)
0 (0.0) 1 (0.47) 0 (0.0) 1 (0.15)
1 (1.59) 2 (0.74) 1 (1.04) 4 (0.50)
1 (0.12) 3 (0.63) 1 (0.60) 5 (0.34)
5 (1.30) 10 (4.74) 7 (10.00) 22 (3.30)
7 (1.59) 27 (10.04) 23 (23.96) 57 (7.07)
12 (1.45) 37 (7.71) 30 (18.07) 79 (5.37)
AD and a case with VaD are presented in Fig. 2. The EEG examinations might be useful for excluding other diseases, but not so helpful in the differentiation of AD from VaD. DISCUSSION A population-based survey among elderly aged 60 years and over was conducted in Sheshan town located in the Southwest suburb of Shanghai with a response rate of over 70%. The majority of the participants in our study were low-educated farmers, and there were more women than men. Generalization of our results should be cautious due to the characteristics of our study participants. For example, a low-educated population may tend to have a relatively higher prevalence of dementia, compared to a high-educated population. In addition, VaD usually occurs more frequently in men [12], which may be determined by other relevant risk factors. We used C-MMSE to identify subjects with CI, which was initially modified by Katzman et al. [13]. The C-MMSE takes around 15–20 minutes to administer, covering various areas of cognitive domains (e.g., orientation, memory, language, and visual construction), and has been proven to be effective in assessing those with different educational backgrounds including illiteracy [13, 14]. According to our previous experience [10], it is appropriate to adjust the cut-
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off points of C-MMSE for the criteria of CI with the educational level, particularly in a low-educated study population. The MMSE is widely used in the screen phase in many epidemiological studies on dementia in the world and is considered a reliable tool to screen for moderate and severe dementia [15]. In the recent decades, a number of studies from China reported prevalence rates of dementia and its major subtypes. A meta-analysis [16] summarized results from 48 surveys on dementia prevalence in China during the period of 1980–2010 and made a pooled prevalence of 3.0% (95% confidence intervals: 2.4%–3.9%) for dementia in the population aged 60 years and over, 1.9% (95% confidence intervals: 1.4%–2.4%) for AD and 0.9% (95% confidence intervals: 0.6%–1.1%) for VaD. Compared to the results from these previous reports in China, prevalence rates of dementia as well as its major subtypes from our study are higher. The difference may be explained in part by the age difference of study participants. Although the mean age for all participants was not described, the pooled prevalence of dementia for participants aged 65 years and over was reported as 6.0% in that meta-analysis [16]. While the mean age of our study participants was 69.67 years. On the other hand, our results are in line with that reported from most world regions, as disclosed by the recently published review and meta-analysis on the global prevalence of dementia, in which most of the estimated agestandardized prevalence rates of dementia were in a range between 5% and 7% for all aged 60 years and over [15]. In our results, AD accounted for around two-thirds, while VaD for one-fourth, of all dementia. The ratio of prevalence between AD and VaD was 2.52, which is almost the same as that (2.50) based on the weighted prevalence of AD and VaD for both genders, reported from the study conducted in four cities in China [5]. In the article with 2,346 cases of dementia from Europe, the ratio of prevalence between AD and VaD was 2.75 [4]. In an article from Japan [17], trends in the prevalence of AD and VaD among elderly over 20 years (1980–2000) were examined. The ratio of the prevalence of AD to VaD increased remarkably over the 20 years, which was attributed by authors to the significantly increased AD prevalence during the period. The classification of AD and VaD may be difficult sometimes, because there are no definite clinical and pathological diagnostic consensus criteria, and the high frequency of mixed pathologies in very old subjects [18, 19]. A definitive diagnosis of AD can only be made with the histopathologic examination of either biopsy
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Fig. 2. Magnetic resonance imaging images for a case with Alzheimer’s disease (AD) and a case with vascular dementia (VaD). A) Female, 78 years, AD. Bilateral hippocampal atrophy and widened parahippocampal sulcus. No significant infarcts observed at the level of the lateral ventricles with T2 W. B) Female, 80 years, VaD. No obvious hippocampal atrophy. Multiple patchy high signals indicating infarcts in the bilateral frontal lobes with T2W.
or postmortem brain tissue [20, 21]. The development of brain imaging techniques during the recent several decades has greatly improved the degree of certainty for diagnosis of dementia. Imaging examinations like CT and MRI are a great help, and 45.9% of all cases with AD or VaD in our study were examined with MRI, which lends confidence about the validity of our classification for cases with AD or VaD. While the diagnosis for dementia is basically clinical, MRI examination is important for the differentiation between AD and VaD. The predominance of females in dementia is observed from most epidemiological surveys. In the meantime, the prevalence rates of dementia and its major subtypes, AD and VaD, are increasing with age [1–5, 16]. Both are valid in the current study. Aging is increasing, especially in China, where the one-child family policy has been effective for more than 30 years. Therefore, it can be expected
that the number of prevalent cases with dementia will increase rapidly in China, which requires a better planning and caring system. In order to wellprepare for and overcome the increasing challenge in China, a nationwide survey and surveillance system on the prevalence of dementia is recommended. As having been commented, such a nationwide survey on the prevalence of dementia is still lacking in the world, particularly in developing countries [15, 22, 23]. In conclusion, the prevalence rates of dementia among elderly from our study are higher than that previously reported from China, but in line with that reported from most world regions. Dementia and its major subtypes, AD and VaD, are more prevalent in women and increasing with age. A nationwide survey and surveillance system on the prevalence of dementia is recommended.
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ACKNOWLEDGMENTS This study was supported by funds from Natural Science Foundation of China (81070958 & 81371218), Shanghai Municipal Health Bureau Key disciplines (12GWZX0101), and Shanghai Science and Technology Commission (07DJ14005). We appreciate the kind support from caregivers of the Community Health Service Centre in Sheshan town and all neurologists, who were involved in the study, at the Department of Neurology, Ruijin Hospital, School of Medicine, Shanghai Jiao Tong University. Authors’ disclosures available online (http://www.jalz.com/disclosures/view.php?id=2000). REFERENCES [1]
[2]
[3]
[4]
[5]
[6]
[7]
[8]
Ferri CP, Prince M, Brayne C, Brodaty H, Fratiglioni L, Ganguli M, Hall K, Hasegawa K, Hendrie H, Huang Y, Jorm A, Mathers C, Menezes PR, Rimmer E, Scazufca M, Alzheimer’s Disease International (2005) Global prevalence of dementia: A Delphi consensus study. Lancet 366, 2112-2117. Prince M, Bryce R, Albanese E, Wimo A, Ribeiro W, Ferri CP (2013) The global prevalence of dementia: A systematic review and metaanalysis. Alzheimers Dement 9, 63-75. Thies W, Bleiler L, Alzheimer’s Association (2013) Alzheimer’s disease facts and figures. Alzheimers Dement 9, 208-245. Lobo A, Launer LJ, Fratiglioni L, Andersen K, Di Carlo A, Breteler MM, Copeland JR, Dartigues JF, Jagger C, MartinezLage J, Soininen H, Hofman A (2000) Prevalence of dementia and major subtypes in Europe: A collaborative study of population-based cohorts. Neurologic Diseases in the Elderly Research Group. Neurology 54, S4-S9. Zhang ZX, Zahner GE, Rom´an GC, Liu J, Hong Z, Qu QM, Liu XH, Zhang XJ, Zhou B, Wu CB, Tang MN, Hong X, Li H (2005) Dementia subtypes in China: Prevalence in Beijing, Xian, Shanghai, and Chengdu. Arch Neurol 62, 447-453. Cui GH, Yao YH, Xu RF, Tang HD, Jiang GX, Wang Y, Wang G, Chen SD, Cheng Q (2011) Cognitive impairment using education-based cutoff points for CMMSE scores in elderly Chinese people of agricultural and rural Shanghai China. Acta Neurol Scand 124, 361-367. American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders, 4th ed., text revised (DSM-IV-TR). American Psychiatric Association, Washington, DC. McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR Jr, Kawas CH, Klunk WE, Koroshetz WJ, Manly JJ, Mayeux R, Mohs RC, Morris JC, Rossor MN, Scheltens P, Carrillo MC, Thies B, Weintraub S, Phelps CH (2011) The diagnosis of dementia due to Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 7, 263-269.
[9]
[10]
[11]
[12] [13]
[14]
[15]
[16]
[17]
[18] [19] [20] [21] [22]
[23]
889
Rom´an GC, Tatemichi TK, Erkinjuntti T, Cummings JL, Masdeu JC, Garcia JH, Amaducci L, Orgogozo JM, Brun A, Hofman A, Moody DM, O’Brien MD, Yamaguchi T, Grafman J, Drayer BP, Bennett DA, Fisher M, Ogata J, Kokmen E, Bermejo F, Wolf PA, Gorelick PB, Bick KL, Pajeau AK, Bell MA, DeCarli C, Culebras A, Korczyn AD, Bogousslavsky J, Hartmann A, Scheinberg P (1993) Vascular dementia: Diagnostic criteria for research studies. Report of the NINDSAIREN International Workshop. Neurology 43, 250-260. Yao YH, Xu RF, Tang HD, Jiang GX, Wang Y, Wang G, Chen SD, Cheng Q (2010) Cognitive impairment and associated factors among the elderly in the Shanghai suburb: Findings from a low-education population. Neuroepidemiology 34, 245-252. Alexopoulos GS, Abrams RC, Young RC, Shamoian CA (1988) Cornell scale for depression in dementia. Biol Psychiatry 23, 271-284. Azad NA, Al Bugami M, Loy-English I (2007) Gender differences in dementia risk factors. Gend Med 4, 120-129. Katzman R, Zhang MY, Ouang-Ya-Qu, Wang ZY, Liu WT, Yu E, Wong SC, Salmon DP, Grant I (1988) A Chinese version of the Mini-Mental State Examination; impact of illiteracy in a Shanghai dementia survey. J Clin Epidemiol 41, 971-978. Zhang MY, Katzman R, Salmon D, Jin H, Cai GJ, Wang ZY, Qu GY, Grant I, Yu E, Levy P, Klauber MR, Liu WT (1990) The prevalence of dementia and Alzheimer’s disease in Shanghai, China: Impact of age, gender, and education. Ann Neurol 27, 428-437. Misiak B, Cialkowska-Kuzminska M, Frydecka D, Chladzinska-Kiejna S, Kiejna A (2013) European studies on the prevalence of dementia in the elderly: Time for a step towards a methodological consensus. Int J Geriatr Psychiatry 28, 1211-1221. Zhang Y, Xu Y, Nie H, Lei T, Wu Y, Zhang L, Zhang M (2012) Prevalence of dementia and major dementia subtypes in the Chinese populations: A meta-analysis of dementia prevalence surveys, 1980-2010. J Clin Neurosci 19, 1333-1337. Dodge HH, Buracchio TJ, Fisher GG, Kiyohara Y, Meguro K, Tanizaki Y, Kaye JA (2012) Trends in the prevalence of dementia in Japan. Int J Alzheimers Dis 2012, 956354. Jellinger KA, Attems J (2010) Is there pure vascular dementia in old age? J Neurol Sci 299, 150-154. Cumming TB, Brodtmann A (2011) Can stroke cause neurodegenerative dementia? Int J Stroke 6, 416-424. Ballard C, Gauthier S, Corbett A, Brayne C, Aarsland D, Jones E (2011) Alzheimer’s disease. Lancet 377, 1019-1031. Mawanda F, Wallace R (2013) Can infections cause Alzheimer’s disease? Epidemiol Rev 35, 161-180. Kalaria RN, Maestre GE, Arizaga R, Friedland RP, Galasko D, Hall K, Luchsinger JA, Ogunniyi A, Perry EK, Potocnik F, Prince M, Stewart R, Wimo A, Zhang ZX, Antuono P, World Federation of Neurology Dementia Research, Group (2008) Alzheimer’s disease and vascular dementia in developing countries: Prevalence, management, and risk factors. Lancet Neurol 7, 812-826. Venketasubramanian N, Sahadevan S, Kua EH, Chen CP, Ng TP (2010) Interethnic differences in dementia epidemiology: Global and Asia-Pacific perspectives. Dement Geriatr Cogn Disord 30, 492-498.
