The symptomatology of Alzheimer's disease: a cross-cultural study

The symptomatology of Alzheimer’s disease:a cross-cultural study

Salman Karim1, Hassan M. Minhas2, Sharmi Bhattacharya1, Kyaw Sein1, Babu Nayar1, Julie Morris3,Asad Nizami2, Fareed Minhas2 and Alistair Burns1

1Psychiatry Research Group, University of Manchester, Manchester, UK2Rawalpindi Medical College, Rawalpindi, Pakistan3Head of Medical Statistics, University Hospital of South Manchester, Manchester, UKCorrespondence to: S. Karim, E-mail: [email protected]

Objective: This paper presents the results of a trans-cultural study looking at the possible differences inthe symptomatology of Alzheimer’s disease (AD) in people from Manchester, UK and Rawalpindi,Pakistan.

Methods: Two groups of people with AD (45 in each group) were recruited at the two sites. Theparticipants and their carers were interviewed to investigate possible differences in demographics andsymptomatology including cognition, depression, personality change and every day activities. Theinstrument used included the Mini Mental State Examination (MMSE), Geriatric Depression Scale(GDS), Cornell Scale for Depression in Dementia (CSDD), The Brooks and McKinlay PersonalityInventory and Informant Questionnaire on Cognitive Decline in the Elderly (IQ CODE).

Results: The data analysis showed that compared to people from Manchester the Pakistanis had lowerliteracy levels but similar cognitive deficits when MMSE scores were adjusted for education. They werehowever more depressed; they had a different profile of personality change since the onset of illness andtheir reported changes in activities of daily living were more severe.

Conclusion: The study has shown a number of possible cultural differences in affective symptoms,personality changes and every day activities. It highlights the need for developing mental health servicesfor older people in Pakistan and making UK services more accessible for this growing community.Further research on service and care needs along with developing culturally sensitive instruments forassessing cognition, psychiatric symptoms, personality changes and daily activities is needed. Copyright# 2010 John Wiley & Sons, Ltd.

Key words: Alzheimer’s disease; activities of daily living; culture; Caucasian; depression; Pakistan; personality; symptomsHistory: Received 21 January 2010; Accepted 16 April 2010; Published online 29 October 2010 in Wiley Online Library(wileyonlinelibrary.com).DOI: 10.1002/gps.2544

Introduction

There is usually a substantial time lag betweenthe first symptoms of Alzheimer’s disease (AD) andthe person coming forward for investigation andtreatment. Prospective follow-up studies havereported a time of 2–6 years, between the onset ofsymptoms and clinical diagnosis (Tierney et al.,1996a,b; Small et al., 2000). A number of earlysymptoms (and signs) have been reported such asshort-term memory loss (Flicker et al., 1991; Chen et

al., 2000), personality changes (Aitken et al., 1999;Smith-Gamble et al., 2002), psychiatric symptoms(Bassiony et al., 2000) and neurological signs(Oppenheim, 1994). The recognition of these earlysymptoms can be influenced by demographic, socio-economic and cultural factors (Moritz and Petitti,1993; Jacobs et al., 1994; Sano et al., 1995; Ross et al.,1997; Cattel et al., 2000).Unfortunately older people from ethnic minorities

are under represented in dementia research and serviceutilization (Lampley-Dallas, 2002). Cross cultural

RESEARCH ARTICLE

Copyright # 2010 John Wiley & Sons, Ltd. Int J Geriatr Psychiatry 2011; 26: 415–422.

studies in dementia, particularly those involvingdeveloping countries, offer opportunities for theunderstanding of the natural history of the diseaseand the various ways in which cultural factors mayinfluence help seeking behaviours.(Hendrie, 1999;Prince et al., 2003). Studies conducted in westernculture on ethnic minorities have reported that they aremore likely to receive a diagnosis at a later stage of thedisease (Guo et al., 2000; Hinton et al., 2000) and tendto use folk models to explain the symptomatology(Levkoff et al., 1999). Shaji (2002) reported that, inIndia, dementia was a hidden problem, considered as anormal part of ageing and not a medical condition,with no community awareness and, despite very highlevels of strain, families often did not seek help. In anepidemiological study in Kerala, India (Shaji et al.,1996), dementia was detected as a major cause ofmorbidity with the families taking the responsibilityof looking after patients. Chandra (1996) reportedthat, in India, older people with memory problemswere rarely taken to a doctor for treatment and carerswere tolerant towards behavioural problems such aswandering. A similar attitude towards memory andbehavioural problems has been reported in Argentina(Mangone, 1996) where people generally consider it apart of aging and seek no medical help. The ‘Countrymental health profile of Pakistan’ (Karim et al., 2004)reported that old age psychiatric services were notdeveloped although elderly population is growing.The Pakistani community is the largest ethnic

minority group in Manchester, comprising about 6.1%(28 100) of the total population of 458 000 (Office ofNational Statistics, 2005). No demographic data isavailable on the exact or estimated numbers ofPakistani people with dementia in Manchester. Arough estimate of about 270 cases could be obtainedfrom the Dementia UK (2007) report that estimatedthe total number of dementia cases inManchester to beabout 4510. Very little work has been done on theservice/care needs of people with dementia belongingto ethnic minorities in general and Pakistanis inparticular. In an audit of prescribing cholinesteraseinhibitors for AD in the North–West of UK, Purandareet al. (2005) reported that of the total number ofpeople on treatment only 3% belonged to ethnicminorities.

Aims

To establish the differences in the symptoms of AD inPakistanis and Caucasians in the domains of cognition,affect, personality and activities of daily living. To our

knowledge, this is the first study to compare thesymptoms of AD in people from Pakistan and England.

Methods

Sample

We studied three groups:

1. Patients with AD of Pakistani origin, living inRawalpindi.

2. Patients with AD of Pakistani origin, living inManchester.

3. Patients with AD of Caucasian origin, living inManchester.

A fourth group (Caucasians from UK settling inPakistan after retirement) was considered but wasfound not to exist.

Setting

In Rawalpindi, there were no existing records ofreferrals or patients known to have AD. Records of GPpractices in the catchment area of the Institute ofPsychiatry were explored for a list of elderly people.Potential participants and their informants wereidentified and approached by local investigators(trained psychiatrists) and screened for dementia onthe basis of informant reports of possible dementiaand Mini Mental State Examination (MMSE) ‘Urdu’version scores.In Manchester, potential participants from the case

records of a Memory Clinic and Local Old AgePsychiatric Services were approached. We encounteredserious difficulties in identifying Pakistani patients inManchester. This arm of the study was dropped as theirnumber was very small (five) and those who wereapproached refused to participate.All potential participants were selected on the basis

of referrals, existing medical records and history.

Inclusion

Those fulfilling the DSM-IV-TR (APA, 2000) criteriafor dementia of the Alzheimer type were recruited forthe study after obtaining written consent. Thediagnosis of AD was made by trained psychiatristsin Pakistan and UK. Ethical approval was obtained


416 S. Karim et al.

from the ethics committees in Manchester andRawalpindi.

Assessments

1. The MMSE, Folstein et al. (1975).2. The 15 item Geriatric Depression Scale (GDS) -

questionnaire to screen for depression in elderly(Yesavage et al., 1983).

3. Cornell Scale for Depression in Dementia (CSDD),a 19-item questionnaire, to assess depressive symp-toms in people with dementia (Alexopoulos et al.,1988).

4. The Brooks and McKinlay personality inventory, forthe assessment of personality change over time(Brooks and McKinlay, 1983), a scale that has beenvalidated in people with dementia. It assesses person-ality change on 18 variables. An informant (spouse/partner or close relative) is asked to give a score, bothfor present and 10 years ago, for each personalityvariable on a five-point scale (�2, � 1, 0, 1 and 2).This provides a comparison or a measure of changein patient’s personality from the way it was 10 yearsago to present. The score difference for each item iscalculated as Inow� I10 years ago where I is a personalityitem. A negative score indicates a personality change.

5. Informant Questionnaire on Cognitive Decline in theElderly (IQ CODE), a 26-item informant question-naire to detect symptom change over time (Jorm andJacomb, 1989). IQ CODE presents a list of everydaysituations where the person has to use their memorysuch as ‘remembering where to find things whichhave been put in a different place from usual’ or‘handling money for shopping’. Each situation israted by the informant for amount of change overthe previous 10 years, using the following scale: 1.Much improved, 2. A bit improved, 3. Not muchchange, 4. A bit worse, 5. Much worse. An averagescore from the 26 items is calculated and scores abovethree are indicative of cognitive decline.

Adaptation of instruments for Pakistani participants

A number of languages including ‘Urdu’, ‘Punjabi’ and‘Potohari’ are spoken in the Rawalpindi region ofPakistan. These languages have many similarities andwe chose to translate the instruments in Urdu, as it isthe national language that is commonly spoken. Weused the ‘Urdu’ version of MMSE (Rait et al., 2000).All the other instruments including GDS, CornellScale, IQ CODE and Brooks and McKinlay PersonalityInventory were translated in Urdu.

Translation protocol

We followed themethod described by Grait et al. (2000)for translating the instruments. We used two separategroups (academics and translators) to review andcomment on the translated instruments. The instru-ments were initially reviewed by the academic group,comprising of experienced psychiatrists, to point outany potential difficulties. They were then translated bythe translator group comprising of professionaltranslators. The translations were then reviewed bythe academic group to back translate and comment onthe meaning and content of the items. The translatorgroup were asked to modify their version in the light ofthe recommendations made by the academic group.The process was repeated until both the groups agreedthat there were no differences between the Englishversions of the modified instruments and the Urdulanguage version. The Urdu versions can be obtained bycontacting the corresponding author.

Sample size and statistics

A power calculation showed that 45 subjects in eachgroup would provide 80% power to detect effect sizesof 0.6 or more between the groups (assuming the useof a t-test with the conventional 5% significance level).This corresponds to differences of 3.6 or more inMMSE (with an SD¼ 6), differences of 2.4 in CSDD(SD¼ 4) and differences in personality item changes of0.9 or more (SD¼ 1.5). Comparisons were made usinga chi-square test, t-test, Mann–Whitney U-test andanalysis of covariance. The GDS scores were logetransformed to produce a reasonable normal distri-bution. All analyses were carried out using the softwarepackage SPSS version 15.0.

Results

Demographics

These are summarized in Table 1. People from Pakistanhad lower literacy levels and the majority werewidowed while the Manchester group were olderand had longer duration of illness and treatment.

Cognition (MMSE)

There was a significant difference between the MMSEscores of the two groups (Table 2, mean difference 4.2,


The symptomatology of Alzheimer’s disease 417

95% CI 1.6–6.8). We examined the relationshipbetween the education level and the MMSE scores.There was a highly significant correlation betweeneducation level and MMSE for the Pakistani group(Spearman correlation¼ 0.42; p¼ 0.004) but not forthe Manchester group (Spearman correlation¼ 0.23;p¼ 0.12). Pakistanis who were illiterate had asignificantly lower mean MMSE score compared tothose who were literate (mean scores 12.9 and 16.3,respectively, p¼ 0.025). The association betweeneducation level and MMSE remained significantfor the Pakistani literate sub-group (Spearmancorrelation¼ 0.54; p¼ 0.01) (Figure 1).On further analyses (analyses of covariance on the

MMSE scores using education level as a covariate) wefound that differences in MMSE scores were notstatistically significant after adjusting for education level.

Depression

On both GDS and CSDD (Table 2) the scores of thePakistani group were significantly higher then theManchester group. The GDS scores were logged

transformed to improve the normality of the distri-bution. On CSDD the majority of people fromManchester (62%) had a score below six, whichsignifies ‘absence of significant depressive symptoms’whereas the majority of people from Pakistan (67%)

Table 1 Description of the samples

Caucasian % (n) Pakistani % (n) p-Value

Total numbers 45 45Male 44% (20) 33% (15) 0.39

Age: mean (range) 78.6 (62, 96) 74.8 (65, 95) 0.02Marital status <0.001Single 7% (3) 0% (0)Married 69% (31) 31% (14)Widowed 24% (11) 69% (31)

Skilled occupation 47% (21) 33% (15) 0.28Education <0.001Illiterate 0% (0) 51% (23)Primary 18% (8) 18% (8)Secondary 60% (27) 22% (10)Graduate 20% (9) 2% (1)Post-graduate 2% (1) 7% (3)

Illness duration (months) median (range) 36 (6204) 26 (8180) 0.025Treatment duration (months) median (range) 24 (6180) 10 (1180) <0.001Family history of dementia 36% (16) 22% (10) 0.24

Table 2 Cognition and depression

Mean (SD) p-Value

Caucasian Pakistani

MMSE 18.7 (7.2) 14.5 (5.2) 0.002MMSE (adjusted for education) 17.5 15.7 0.21GDS (geometric mean, range) 1.7 (0.11) 6.5 (4.8) <0.001CSDD 5.0 (3.1) 14.4 (5.2) <0.001

Figure 1 Relationship between education level and MMSE.


418 S. Karim et al.

had a score in the 10–18 ranges signifying ‘probablemajor depression’. On Pearson correlations there was astatistically significant positive relationship betweenGDS and CSDD for Caucasians (r¼ 0.55; p< 0.001)but not for Pakistanis (r¼ 0.25; p¼ 0.10).

Personality (Brooks and McKinley personalityinventory)

The mean change scores for each of the 18 items werecompared between the two groups (Table 3). TheCaucasians and Pakistanis demonstrated a similarpattern of change with negative mean scores (indicat-ing personality change) for 10 and 11 items,respectively. On comparison, there were statisticallysignificant differences on eight items (2, 3, 8, 9, 10, 11,12 and 17) between the two groups.

Reported every day activities

The scores of the two groups on the IQCODE aresummarized in Figure 2. The difference in medianscores for Pakistanis 4.69 (range: 3.23–5.00) andCaucasians 4.27 (range: 3.77–5.00) was statisticallysignificant (Mann–Whitney test: p< 0.001). We alsolooked at the individual item scores and found thatpeople from Pakistan scored higher than those fromManchester on all items apart from three items (5, 8and 10) In 11 items the differences were statisticallysignificant, indicating an overall greater decline inPakistanis in every day activities (Table 4).

Discussion

We compared, for the first time as far as the authors areaware, mood personality changes and reportedactivities of daily living in people with AD from twodifferent cultures. There were three main findings:people from Pakistan with AD were more depressed;they had a different profile of personality change sincethe onset of illness; and their reported changes inactivities of daily living were more severe.The Pakistanis, based on theMMSE scores, appeared

significantly more impaired although Caucasians wereolder and had longer duration of illness. This differencehowever was not statistically significant after adjusting

Table 3 Personality changes

Personality variable Pakistani Caucasian p-Value

Mean SD Mean SD

1. Talkative/quiet �0.78 2.07 �1.30 1.44 0.1732. Even tempered/quick tempered �0.11 1.70 �0.80 1.55 0.0473. Reliant on others/does things himself 2.11 1.65 1.36 1.85 0.0444. Affectionate/cold �0.78 1.66 �0.64 1.23 0.6665. Likes company/dislikes company �0.73 1.56 �0.73 1.05 1.0006. Irritable/Easy going 0.71 1.65 0.58 1.57 0.6957. Unhappy/happy 1.38 1.45 0.622 1.72 0.0278. Excitable/calm �0.71 1.69 0.27 1.05 0.0029. Energetic/lifeless �1.71 1.24 �0.91 1.46 0.00610. Down to earth/out of touch �0.04 1.36 �0.98 1.39 0.00211. Rash/cautious 0.98 1.62 0.16 1.19 0.00712. Listless/enthusiastic 1.27 1.30 0.78 1.57 0.11113. Mature/childish �1.40 1.74 �0.93 1.45 0.17014. Sensitive/insensitive �0.78 1.43 �0.64 1.43 0.65915. Cruel/kind 0.31 1.53 0.20 0.81 0.66916. Generous/mean �0.20 1.62 �0.47 1.10 0.36317. Unreasonable/reasonable 1.31 1.22 0.40 1.30 0.00118. Stable/changeable �0.93 1.34 �1.22 1.59 0.354

Figure 2 Activities of daily living.



for education levels. There was a significant correlationbetween education level and MMSE for both literateand illiterate Pakistani sub-groups. Moreover theilliterate Pakistanis had a significantly lower MMSEscore than the literate group. Similar findings havebeen reported regarding the influence of culture andeducation on the use of translated versions ofMMSE innon-western cultures (Espino et al., 2001; Mehta et al.,2004; Wood et al., 2006).The Pakistani group had significantly higher

depression scores and on CSSD their mean scorewas in the ‘probable major depression’ range. A widerange of prevalence figures for depression in AD havebeen reported with most ranging between 30 and 50%(Olin et al., 2002). The reported range is wider, 3.5–39.6%, in African and Cuban ethnic minorities andChinese cultures (Liu et al., 1999; Harwood et al.,2000a,b). Our findings might reflect cultural differ-ences in symptoms of AD although other factors suchas carers and referral bias or simply lack adequatepsychiatric services might have contributed. They may

also reflect an overall higher prevalence of depression(34%) in Pakistani society linked to adverse socio-economic and political circumstances as reported in asystematic review by Mirza and Jenkins (2004).The personality changes within the two groups have

shown significantly different patterns. Overall, Cau-casians became more quick-tempered, excitable andout of touch. The Pakistanis became unhappier, calm,lifeless, reliant on others, rash and unreasonable.Higher levels of depression in Pakistanis could explainsome of these differences but it is possible that they aredue to cultural differences. Other studies have alsoreported cultural differences such as Hendrie (1999)compared personality changes in African Americans,Jamaicans and Nigerian AD patients. They reported ahigher degree of overall personality change along with arelative increase in stubbornness, irritability and angerin African Americans as compared to the other twogroups.Both groups showed a decline on activities of daily

living but the Pakistani group was significantly more

Table 4 Activities of daily living

Caucasians Pakistanis p-Value

Medianscore

% Muchworse

Medianscore

% Muchworse

1. Recognizing the faces of family and friends 3 16 4 31 0.0082. Remembering the names of family and friends 4 29 5 53 0.143. Remembering things about family and friends,e.g. occupations, birthdays and addresses

5 58 5 64 0.58

4. Remembering things that have happened recently 5 69 5 71 0.775. Recalling conversations a few days later 5 80 5 71 0.226. Forgetting what he/she wanted to say in themiddle of a conversation

5 51 5 76 0.011

7. Remembering his/her address and telephone number 4 36 5 67 <0.0018. Remembering what day and month it is 5 78 5 78 0.879. Remembering where things are usually kept 5 60 5 69 0.3210. Remembering where to find things put in adifferent place from usual

5 84 5 78 0.41

11. Adjusting to any change in his/her day-to-day routine 4 36 5 60 0.02512. Knowing how to work familiar machines around the house 4 44 5 78 <0.00113. Learning to use a new gadget or machine around the house 5 69 5 80 0.1214. Learning new things in general 5 71 5 76 0.6115. Remembering things that happened when young 3 11 4 11 0.0716. Remembering things learned when young 3 18 4 24 0.01617. Understanding the meaning of unusual words 4 33 5 78 <0.00118. Understanding magazine or newspaper articles 4 31 5 80 <0.00119. Following a story in a book or on TV 4 49 5 71 0.02820. Composing a letter to friends or for business purposes 5 56 5 80 0.00921. Knowing about important historical events of the past 4 22 4 44 0.01622. Making decisions on everyday matters 5 71 5 82 0.2223. Handling money for shopping 5 53 5 82 0.00324. Handling financial matters, e.g. the pension,dealing with the bank

5 69 5 89 0.030

25. Handling other everyday arithmetic problems,e.g. knowing how much food to buy etc

5 62 5 87 0.005

26. Using intelligence to understand what is going onand to reason things through

4 40 5 82 <0.001


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impaired both on combined scores and individualscores in all except three domains. The possibility ofsevere depressive symptoms, lack of drive and energyaffecting patient’s ability to perform activities needs tobe considered while interpreting these results. In theabsence of a significant difference in cognition thesefindings may also suggest that educational and culturaldifferences might be responsible for them. Looking atthe individual items of IQ CODE it is apparent thatsome activities are dependent on the individual’seducational level such as ‘understanding magazine ornewspaper articles’, ‘following a story in a book’ and‘composing a letter to friends or for business purposes’.However they also scored low on other items which donot appear to be dependent on education such as‘recognizing the faces of family and friends’, ‘adjustingto any change in day-to-day routine’, ‘rememberingthings they learnt when young’, ‘knowing how to workfamiliar machines’, ‘handling money for shopping’,‘handling other everyday arithmetic problems’ and‘using their intelligence to understand what is going onand to reason things through’. Overall the results needto be interpreted in the light of IQ CODE beingdeveloped for use in western culture and weather otherinstruments such as CSI-D (Hall et al., 1993) mighthave been more appropriate for assessing activities ofdaily living in trans-cultural setting.In summary, this study was an attempt to look at the

cultural differences in the presentation of AD inPakistanis and Caucasians. It has shown a number ofpossible cultural differences in affective symptoms,personality changes and every day activities. Our studyhighlights the need for developing mental healthservices for older people in Pakistan and making UKservices more accessible for this growing community.Further research on service and care needs along withalong with developing culturally sensitive instrumentsfor assessing cognition, psychiatric symptoms, person-ality changes and daily activities is needed.

Conflict of interest

None declared.

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Key Points

� In a transcultural study of symptomatology ofAlzheimer’s disease, the authors compared moodsymptoms, personality changes and activities ofdaily living in people with AD from two differentcultures (England and Pakistan). There were threemain findings: people from Pakistan with AD weremore depressed; they had a different profile ofpersonality change since the onset of illness; andtheir reported changes in activities of daily livingwere more severe.



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The symptomatology of Alzheimer's disease: a cross-cultural study

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