The Arab world will have a rapidly aging population in the next few decades 1. The anticipated increase in Egyptian individuals older than 60 years of age is from 6 to 11.5% by the year 2025 2 and this increase will exert a profound impact on the mental healthcare system 3.
Although older patients with late-onset schizophrenia (LOS) represent a minority (2–4%) among the elderly population 4,5, they account for a disproportional amount of services and costs 6.
‘Late-onset schizophrenia’ was first described and defined by Manfred Bleuler in 1943 as a form of schizophrenia with manifested onset of symptoms after the age of 40 years 7. Systematic studies in this field continued in Germany and other European countries 8,9.
In the UK, psychiatrists often used the term ‘Late-onset paraphrenia’ interchangeably with ‘Late-onset schizophrenia’ to designate this disorder. However, late-onset paraphrenia is a British concept that includes all delusional disorders starting after the age of 60 years 8,10. American psychiatrists paid little attention to this patient group; thus, it is only within the Diagnostic and Statistical Manual of Mental Disorders, 3rd ed., Revised (DSM-III-R) that a separate category was created for patients who developed schizophrenia after the age of 44 years 11. Currently, there is no longer a ‘late-onset’ category for either schizophrenia or an age criterion for the diagnosis of schizophrenia in the DSM-IV 12, nor International Statistical Classification of Diseases and Related Health Problems, tenth revision (ICD 10) 13. In the French nosography, schizophrenia is excluded when a nonaffective, nonorganic psychosis begins after the age of 40 years. These chronic delusion syndromes fall into a specific French category: ‘Psychose Hallucinatoire Chronique’ (chronic hallucinatory psychosis) 14.
In their review, Vahia et al. 11 reported that there is still opportune time to consider available empirical data to place LOS in the development of ICD11 or DSM-V as a subtype of schizophrenia.
In the year 2000, an international consensus was established with respect to a specific definition and research questions; the consensus assigned LOS to schizophrenia or to a related disorder, for example schizoaffective, schizophreniform, or delusional disorder after the age of 50 years 15 and with women predominance.
Paranoid subtype of LOS is the most common subtype, with less severe negative symptoms, less cognitive impairment, and a better prognosis compared with those who are diagnosed at a younger age 15–17.
There are still conflicting reports on the epidemiology of LOS 15. The proportion of schizophrenic patients whose illness first emerges after the age of 40 years in the absence of dementia or primary affective disorder has been estimated to be about 23% 16 to 25% 18,19. The possible risk factors contributing toward LOS have been reviewed extensively by different workers. who pointed to female sex, being isolated, and having sensory deficits 15,19–22.
Although there is a general agreement on the presence of neuropsychological impairment accompanying LOS, there have not been many attempts to identify and characterize the profile of cognitive and functional impairments of these patients 6,23,24.
Hopkins and Roth 25 were the first investigators to study cognitive deficits in LOS; however, their attempts were limited because of the absence of a control group.
Knowledge is still sparse and controversial on the cognitive profile and functioning of these patients 17,26,27.
Little is known about this problem in Egypt, where increasing longevity 2 may be associated with the risk of increased medical, psychiatric, and behavioral problems in the elderly population 3,28.Thus, there is a great need to implement mental health plans for elderly Egyptian patients with LOS.
We consider this study as an essential step for the guidance of mental health professionals in order to streamline comprehensive recommendations, aiming to minimize the costs of this devastating disorder.
Aim and ethical considerations
This study focuses on the cognitive deficits and impairment in daily functioning that results from the illness rather than those that occur as a result of normal aging. This will help to achieve a better understanding of the illness and to better respond to the needs of this largely neglected group.
The research protocol was approved by the Ethical and Research Committee of Ain Shams University. Written informed consent from patients or their legal substitute was obtained by the appointed researchers, who discussed the study protocol with the patients, ensured the confidentiality of the information provided, and assured the patients that they were free to participate in or withdraw from the study at any time.
Patients and methods
The study design was a cross-sectional comparative study and the sample was selective. A total of 100 candidates were recruited over a 1-year period from March 2008 to February 2009; they were selected as follows:
- Group 1 included 50 patients with LOS. We used also the operational definition according to the consensus statement by the International Late-Onset Schizophrenia Group, which stated that the term could be applied to those patients with onset of prodromal symptoms after the age of 50 years and refers to schizophrenia or a related disorder (schizoaffective, schizophreniform, or delusional disorder) 6,15,20. All patients, both men and women, fulfilled the diagnostic criteria of schizophrenia and other psychotic disorders according to the DSM-IV classification. They were recruited from among the inpatients and outpatients attending the Geriatric Hospital and Institute of Psychiatry, Ain Shams University Hospitals. Some patients were also recruited from the Abbasseya state mental Hospital because of the rarity of patients. All patients enrolled in the study had to have developed schizophrenia after the age of 50 years; patients should neither have a lifetime history of schizophrenia, other psychoses including (schizoaffective disorder, paranoid disorder), nor psychotic symptoms secondary to other mental or general medical disorders or dementia. All patients were under psychotropic medication to enable them to engage in the process of interview.
- Group 2 included 50 apparently mentally healthy control male and female participants (older than 50 years of age) who were matched for age and sex with (group 1) and were recruited from among the relatives of patients attending the inpatient and outpatient clinics of the Geriatric Ain Shams University Hospital. Before inclusion in the study, the apparently healthy individuals recruited were asked to fill out the Arabic version of the General Health Questionnaire 29 translated by Okasha 30. The General Health Questionnaire is a self-administered screening questionnaire designed by Goldberg 29 for use in consulting settings aimed at detecting those with a diagnosable psychiatric disorder. Any participant with a score of 7 or more (cut-off points in Egyptian population) might have had minor psychiatric morbidity, and was thus excluded from the study.
- All consenting individuals in each study group who fulfilled the research criteria were subjected to a preliminary evaluation of history of illness, obtained from the patient and his/her companions. A specialist gerontologist performed the physical and neurological examination of all enrolled individuals. Before inclusion in the study proper, all patients were interviewed by the researchers using the Structured Clinical Interview for DSM Axis-I Disorders 31, which is a semistructured, clinician-administered interview that was developed to provide broad coverage of psychiatric diagnosis according to DSM-IV 12. Most diagnoses are made on a lifetime (ever present) and current (fulfilled diagnostic criteria in the past month) basis and are recorded on the summary score sheet at the beginning of the Structured Clinical Interview for DSM Axis-I Disorders. Diagnoses are made by the interviewer during the course of the interview.
- Reviewing medical files: medical data were collected from the patient’s hospital files and reviewed by the research team.
Both the patient (group 1) and the control group (group 2) were assessed comprehensively as follows.
Sociodemographic data were assessed using the social classification scale in an Egyptian community 32.
Assessment of daily functioning
Activities of daily living 33
This assesses certain basic abilities that an individual must possess to remain at home independently. These abilities allow an individual to perform basic self-care tasks. Accordingly, patients were classified as follows: needs no support (10), needs partial support (6–9), or needs full support (0–5). The Arabic standardized version was used 34.
Instrumental activities of daily living 33
This scale measures two broad categories: (a) basic self-maintenance behaviors such as feeding, dressing, bathing and mobility and (b) more complex behaviors such as managing finances, traveling, and taking medications. These abilities are higher level abilities that allow an individual to function independently at home or in the community. Accordingly, patients were classified as follows: needs no support (10), needs partial support (6–9), or needs full support (0–5). We used the Arabic standardized version 34.
Cognitive assessments using the Cambridge Mental Disorders Of The Elderly Examination scale 35
We used section B of the scale (CAMCOG), which was developed to assess the diagnosis and measurement of dementia in the elderly. This scale assessed orientation, language (expression, comprehension), memory (recent and remote), learning, praxis, attention, abstract thinking, perception, and calculation. It was translated into Arabic and validated by Mahmoud 36.
All measures were administered by the researchers, who had completed training for several months on the tools and showed a high inter-rater reliability before performing the evaluations.
Neuropsychological assessment using the Wechsler Adult Intelligence Scale 37
The Wechsler Adult Intelligence Scale (WAIS) is viewed as a tool for the broad assessment of cognitive functions that provides information about the important aspects of an individual’s intellectual functioning such as comprehension, arithmetic, similarities, vocabulary, digit span, picture completion, block design, and digit symbol. We used the standardized Arabic version 38.
The WAIS was administered to all candidates by a consultant psychologist who had proper working experience with the use of WAIS.
Data processing and statistical analysis
Statistical analysis was carried out using the statistical package for social sciences software, version 17.0 (SPSS v. 17, Inc., Chicago, Illinois, USA). Descriptive statistics were calculated as means and SD for numerical parametric data, whereas number and percentage were calculated for categorical data. Inferential analyses were carried out for quantitative variables using the Student t-test for two independent groups. Qualitative data were analyzed using the Pearson χ2-test. The level of significance was considered at P value less than 0.05; otherwise, it was nonsignificant.
We compared the two groups with each other in terms of their sociodemographic characteristics, activities of daily living (ADL), and cognitive functioning.
The mean age of the patients in group 1 was (69.5±3.39) years; they developed their first onset of schizophrenia symptoms at the mean age of (57.24±6.6) years and they had schizophrenia for (12±3.4) years; however, they did not consult mental health professionals at the onset of the illness. The majority (70%) were diagnosed with paranoid schizophrenia, whereas 14% had schizoaffective disorder and 12% had delusional disorder and only 4% had undifferentiated schizophrenia; details of the clinical characteristics have been described in the study by Mahmoud et al. 22.
Data shown in Table 1 indicated no statistically significant differences between group 1 and group 2 in age, sex, education, previous occupation, or social class because the control group was matched with the study group as much as possible. It is clear from Table 1 that there is a preponderance of women (72%) compared with only 28% of male patients.
Despite insignificant differences between the levels of education in both groups (P=0.59), the participants in group 2 tended to be more illiterate and they could only read and write compared with the participants in group 1, who had received mainly secondary school education.
Significantly more patients with LOS (group 1) were never married or divorced, and living alone compared with the elderly healthy controls (group 2), who were married or widowed and living with their spouses and children (Table 1). The patients in group 1 showed insignificantly higher prevalence of a positive family history of psychiatric disorders than the participants in group 2 (Table 1).
The patients of group 1 had significantly (P=0.000) more chest diseases (72%), auditory impairment (30%), musculoskeletal problems (66%), and gastrointestinal (GIT) diseases (50%) compared with the controls. No statistically significant difference was found between the two groups in diabetes mellitus, hypertension, cardiac diseases, neurological disease, renal diseases, and visual impairment (Table 1).
Functional assessment of daily living
Data showed nonsignificant differences between both groups (groups 1 and 2) in the scores obtained in the ADL and instrumental activities of daily living (IADL) assessments (Table 2).
Yet, 4% of patients with (LOS) needed complete support in ADL and 8% needed partial support compared with 0 and 6%, respectively, of the participants in the control group (P=0.98).
Also, in IADL, 4% of the patients needed complete support and 16% needed partial support compared with 0 and 12%, respectively, of the controls (P>0.05).
Using section B in CAMGOG of the Cambridge Mental Disorders Of The Elderly Examination scale, it was found that the patients in group 1 scored significantly worse in the total CAMGOG scores and in the following subitems: perception, abstract, apraxia, memory, and language than did the healthy controls. However, there were no statistically significant differences between the two groups in attention and orientation scores (Table 3).
Data of the WAIS showed that the patients of group 1 scored lower on the total scores and most of the subitems of WAIS, except digit symbol code, than did participants in group 2 (Table 4).
Psychotic symptoms arising in the elderly are of increasing clinical interest 15 and may be more common than was considered previously 17,39; there is clearly an enormous need to clarify this issue among our elderly Egyptian patients as this topic remains poorly understood and investigated.
The current study was designed to assess demographic data, cognitive, and daily functions of patients with LOS compared with age-matched and sex-matched healthy controls, with the intention that the data obtained would be useful to the mental healthcare authority.
Our results showed that the ratio of women to men was almost 3 : 1, which replicates previous studies that showed a female preponderance among patients with LOS 6,21.
This sex disparity can be attributed to several factors, including neuroendocrine changes (estrogen hypothesis), which relates the risk of late-onset psychosis in women to the decrease in estradiol levels during the menopausal period along with associated excess of dopaminergic functions 23,40. Estrogen has been postulated to confer some protection from psychosis before menopause; however, definite evidence for this hypothesis is lacking 12,41. Other factors that contribute toward sex differences in LOS include psychosocial stressors and different role expectations 21.
Social isolation has been cited as a factor that may predispose to psychosis in later life 6,11,42.
Our results showed that 54% of patients were never married and 62% were living alone compared with 56 and 4%, respectively, of the controls. In a different culture, Almeida et al. 19 reported that 79% of the participants were socially isolated. The differences in the results could be attributed to cultural differences, as in Egypt, the elderly often live with their extended families, especially in rural areas.
Sensory impairments as well as visual and hearing loss have been proposed in a number of studies as possible etiological factors in the emergence of auditory and visual hallucinations and psychosis 14,23,43. The current study estimated that the risk of auditory impairment is five times greater than that in the matched controls. However, our results are in agreement with those of some previous investigations, that is, the mechanisms explaining how sensory impairment could produce psychiatric illness are unclear 19,44.
As both the studied groups were matched in age and sex, they had very similar medical profiles, except that LOS patients had higher rates of respiratory morbidity; this could be attributed to the excessive smoking usually reported in patients with schizophrenia 45,46. LOS patients are less physically fit than their healthy counterparts. The higher rates of musculoskeletal and GIT problems in our patients may contribute toward their difficult mobility, and hence their social isolation; also, the frequency of GIT complaints may probably be related to the use of NSAIDs.
In our study, we found a lower prevalence of family loading of schizophrenia among family members of patients with LOS compared with matched controls.
In contrast to our finding, some investigators found that more family members of LOS patients had schizophrenia 23,47,48.
Our results are in agreement with those of many previous researches reporting that hereditary factors are less influential in the development of LOS 49.
In a previous a Egyptian study carried out by Fawzi 50, it was found that patients with LOS had less familial aggregation than patients with early-onset schizophrenia. Recently, Köhler et al. 26 reported that LOS constitutes a separate phenotype within the schizophrenia spectrum.
Assessment of daily living functioning
Inability to function in everyday settings is responsible for the huge indirect costs of early-onset schizophrenia 46. In contrast, patients with LOS were more likely to have little association with impaired everyday functioning 11,51. This is the case in the current study, in which assessment of daily functioning showed that our patients with LOS had insignificantly higher ADL and IADL scores compared with the healthy matched controls. Thus, these patients can maintain independence in residential functioning.
Cognitive deficits in schizophrenia are core features of the illness and are believed to be a manifestation of a process affecting different brain functions 27,52.
In the current study, patients with LOS performed significantly worse than healthy controls on measures of global cognitive functions; our results are in agreement with those reported by previous investigators 6,15,27,46.
Language and verbal functions
Regarding our LOS patient’s vocabulary and language abilities are inconsistent with the work carried out by Paulsen et al. 53, and Rajji et al. 27, who assessed the semantic organization in patients with LOS and reported that these functions were preserved. However, our results are in agreement with those of Mueser et al. 54, who concluded that vocabulary and language functions were significantly worse in LOS patients than their healthy counterparts. Verbal functions, pragmatic errors, and a dysfunctional semantic system have been suggested as possible origins of formal thought disorder and impaired communication in LOS patients 55,56.
Our patients with LOS scored significantly lower than controls on the memory subscale of CAMCOG and the digit span test of Wechsler, which reflect visual and auditory memory functioning.
In agreement with our results, Rajji and Mulsant 57 reported that memory functions were consistently impaired in LOS.
Results on attention were more conflicting; no deficit in attention could be elicited in our LOS patients compared with matched healthy controls. The present findings are in contrast to those of Rajji et al. 27, who concluded that patients with LOS have more impaired auditory, visual attention, and visuospatial construction. The inconsistency between these findings in cognitive dysfunctions in LOS may be because of the different methodology and inclusion criteria.
In this study, LOS patients and controls had preserved digit symbol code, which reflects immediate memory and visuomotor coordination. Similar findings have also been reported by previous studies 6,27.
The slight deficit in the digit symbol code is of particular interest as performance on this task is considered to depend on a nonspecific neurological process and correlated with prefrontal and temporal gray matter volume. Thus, the preservation of this task suggests a specific rather than a generalized cognitive deficit in LOS 58.
Arithmetic, praxis, and perceptual functions
LOS patients showed poor arithmetic and praxis abilities and worse perceptual functions (as measured by block design and CAMCOG), in addition to poor abstraction (as estimated by similarities). Our results are in partial agreement with the findings reported by Gold et al. 59 and Heinrichs and Zakzanis 60.
The current study found that patients with LOS had little impairment in daily living functioning; however, they showed significant global cognitive impairments compared with the general population of the same age group that is not accounted for by the simple aging process. The insights gained from the current research may lead to a broader understanding for this disorder in this neglected group and may direct efforts for future provision of services aiming to decrease the emotional and financial burden of caring for these patients.
Strength, limitations, and recommendations
The study provides useful information on this poorly understood and underinvestigated area of research in Egypt. However, the data obtained should be considered preliminary data because of the limitations of the small size taking into consideration the difficulty in recruiting LOS patients; the second limitation is the type of sample, which was a selective rather than a stratified random sample. The third limitation is that the majority of LOS patients enrolled were being treated with antipsychotics, which could impair their cognitive functions. Furthermore, longitudinal studies are needed to improve our knowledge of the cause–effect relationship. Future studies should encompass different geographical regions in Egypt.
The authors are grateful to Professor Afaf Hamed Khalil, Professor of Psychiatry, for her guidance and advise and Dr Mahmoud Tamara, Geriatric Medicine Department, for his efforts in the recruitment of cases. The authors are also grateful to Dr Hisham Sadek, Dr Abeer Mahmoud, Dr Hanan Hussien, Dr Ahmed El Shafeiy, Dr Marwa Abdel Meguid, and Dr Marwa Elmissiry for their efforts in training on tools and reviewing of the medical files.
The authors thank Dr Olfat Kahla, senior psychologist in Geriatric Hospital, for her efforts and the psychometric assessment; we also thank Dr Mohamed Hassan Taha from TIT solution for the statistical analysis. Last but not least, the authors thank every participant enrolled in this study and their families for their participation, time, and effort.
Conflicts of interest
There are no conflicts of interest.
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