Department of Psychiatry, Nara Hospital, Kinki University School of Medicine, 1248-1 Otodacho, Ikoma City 630-0293, Japan
Copyright © 2012 Akira Okada and Junko Matsuo. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Highly emotional events in daily life can be preserved in memory and such memory is generally referred to as emotional memory. Some reports have demonstrated that emotional memory is also found in patients with Alzheimer’s disease (AD). However, to our knowledge, there have been no reports about how long memory retention for emotional events can continue in patients with AD. In this paper, we present two patients with AD who lost an immediate family member during followup and retained the memory over a long period despite progression of the AD.
The study of emotional memory in patients with Alzheimer’s disease (AD) takes two general paths. The first involves the use of photographs, words, and stories to investigate delayed recognition memory for emotional stimuli in an experimental setting. Several such studies have found emotional enhancement effects in AD [1–3], but there is some debate over the effects of emotional content on memory . The second involves an investigation of the real-life experiences of patients with AD. One such study looked at experiences of the great Hanshin-Awaji earthquake in Japan in 1995 . The findings revealed that subjects better remembered the earthquake than a magnetic resonance imaging (MRI) examination performed after the earthquake (mean interval of 59.2 days between the earthquake and memory survey versus 17.5 days between the MRI examination and survey). In addition, they recalled personal events during the earthquake well but nonpersonal, factual knowledge poorly. These studies provide findings that are extremely useful to our understanding of AD, but to our knowledge, there have been no reports about how long memory retention for emotional events can continue in patients with AD.
In this paper, we present two patients with AD who lost an immediate family member during followup and retained memory of the event over a long period despite progression of the AD. Both patients’ families provided verbal informed consent to publish the cases, with due consideration given to protecting the patients’ identities.
2. Case Presentation
2.1. Case 1
Case 1 was a 75-year-old woman who visited our hospital with her son due to her insistence that her bag had been stolen, but for around two years she had often misplaced her bag or purse. She had no history of psychiatric disorders.
At the initial visit, no abnormal findings were found on routine blood tests, hematochemistry, or electroencephalography. Magnetic resonance imaging (MRI) of the brain showed no cerebrovascular damage, organic change, or striking atrophy. Her mini-mental state examination (MMSE)  score was 20 (orientation to time 2/5, orientation to place 2/5, registration 3/3, attention and calculation 5/5, recall 1/3, naming 2/2, repetition 1/1, following commands 3/3, reading 1/1, writing 0/1, and design copy 0/1). We gave a diagnosis of stage 4 AD (mild dementia) using the functional assessment staging (FAST) tool . She was started on donepezil 5 mg/day and returned for follow-up visits with her son about once a month. Just over two years (26 months) after her first visit, she began to use elderly day care services and 17 months later she could not do simple calculations or shop alone. At five and a half years months after the first visit, she travelled abroad with her family, but had no recollection of the trip three weeks after returning to Japan. Then at just over seven years after her first visit, her son died of kidney cancer. Three weeks later, she said, “My son died. I wanted to pass away earlier than him,” but she could not accurately remember factual knowledge about the funeral or Buddhist services she attended (e.g., approximate number of people at the funeral, place of the funeral home, and number of Buddhist services). We rated her at FAST stage 5 (moderate dementia) at this time. Eight and a half years after the first visit, she was assessed to be at FAST stage 6.6 (moderately severe dementia characterized by improperly putting on clothes, difficulty adjusting bath-water temperature, forgetting to flush the toilet, and urinary incontinence) and increased the dose of donepezil to 10 mg/day. Three years later (137 months after first visit), she verbally expressed the same feeling as shortly after her son had died. Two weeks later, she was admitted to our hospital because of loss of consciousness. MRI examination of the brain on admission showed no cerebrovascular damage or organic change but there was enlargement of both lateral ventricles. She died of cardiac failure after two days in hospital.
2.2. Case 2
Case 2 was a 65-year-old woman who visited our hospital with her husband because she had developed feelings of anxiety and sleep disturbance after visiting her mother in hospital. She had become unable to cook, make telephone calls, and shop without assistance for two years. She had no history of psychiatric disorders.
At the initial visit, there were no abnormal findings on routine blood tests or hematochemistry. Brain MRI showed no cerebrovascular damage, organic change, or striking atrophy. Her MMSE score was 18 (orientation to time 3/5, orientation to place 4/5, registration 3/3, attention and calculation 1/5, recall 0/3, naming 2/2, repetition 1/1, following commands 3/3, reading 1/1, writing 0/1, and design copy 0/1). We gave a diagnosis of AD, FAST stage 4 (mild dementia). She was given donepezil 5 mg/day and returned for follow-up visits with her husband around once a month. Feelings of anxiety and sleep disturbance showed improvement at the two-month follow-up visit.
Twenty months after the first visit, her mother died. Eighteen days later, she said “I miss my mother. I want someone to be around me.” Like Case 1, she could not accurately remember factual knowledge about the funeral and Buddhist services she attended. Her diagnosis was FAST stage 4 (mild dementia) at this time. Three years after the first visit, she very often forgot to turn off taps and electrical equipment, and medication noncompliance was suspected. Six months later, brain MRI showed no cerebrovascular damage or organic change but did show enlargement of both lateral ventricles. 123I-IMP brain single photon emission computed tomography showed symmetrical decreased cerebral blood flow in bilateral temporal and parietal lobes. She was judged to be at FAST stage 6.4 (moderately severe dementia characterized by improperly putting on clothes, difficulty adjusting bath-water temperature, and forgetting to flush the toilet) and donepezil was increased to 10 mg/day. Five years after the first visit, she often experienced nocturnal delirium after nontypical events such as dental treatment. Four months later (64 months after first visit), she was admitted to a special nursing home for the elderly. Ten days before admission, her MMSE score was 5 and she verbally expressed the same feeling as when her mother had died.
In the two cases presented, we noted four interesting findings. First, emotional memory was found to be intact at FAST stages 4 (mild) and 5 (moderate) in our two patients with AD. They expressed feelings of desolation and loneliness at 20 days and 18 days, respectively, after their immediate family member had passed away even though they often forgot notable life events that had taken place just a few days earlier. In general, AD is a slowly progressive disease caused by atrophy of the medial temporal lobe including the amygdala, which is thought to play a crucial role in emotional memory . Therefore, it is speculated that the progression of AD possibly undermines the effects of emotional arousal on memory. Our cases suggest that such effects may not be undermined until beyond FAST stage 5 in patients with AD.
Second, marked emotional arousal was effective for retaining memory of their immediate family member dying but not for retaining factual knowledge about the funeral or Buddhist services. This is consistent with the finding reported for patients with AD that experienced the great Hanshin-Awaji earthquake mentioned above .Emotional memory enhancement might therefore have greater effect on episodic memory than on semantic memory in patients with AD.
Third, emotional arousal was caused by an extreme negative event. In Case 1, before the son’s death, it had not been triggered by overseas travel, which can be considered to be positive in terms of emotional valence. This suggests that negative real-life events that cause psychological distress, such as losing a family member, might easily produce greater emotional enhancement effects than positive events in patients with AD.
Lastly, we know from experience that a favorable environment is helpful in managing patients with AD. Both of our patients retained memory of their family member’s death even at FAST stage 6 (moderately severe dementia), indicating that patients with AD may retain memory for highly negative events over a long period even with disease progression.
In conclusion, these two cases suggest that patients with AD may preserve the ability to store negative events for long periods, until at least FAST stage 5. These findings indicate that memory of experiences in an unfavorable care environment, such as an abusive one, may be retained in the memory of patients with AD. More reports of cases are needed to clarify the nature of emotional memory in AD.
As mentioned earlier, Alzheimer’s disease is of extreme importance. The care for patients might be divided into outpatient and inpatient care. These two approaches involve totally different practices and consequently different costs and demands of other resources.
Outpatient care and its costs
In 2012, 15,352 patients with the diagnosis of F00 (dementia in Alzheimer’s disease) and 21,279 patients with the diagnoses of F01–F03 (other dementias) were treated in outpatients facilities in the Czech Republic.2
Based on the investigation of the research team in the University Hospital in Hradec Králové, data were obtained through a guided interview with the Head of the Department of Neurology. Moreover, the outcomes were supported by the real data obtained from the Department of Neurology.6 Hort et al7 provided recommendations for clinical diagnoses; blood tests; neuropsychology, neuroimaging, electroencephalography, and cerebrospinal fluid (CSF) analysis; genetic testing; disclosure of diagnosis; treatment of Alzheimer’s disease; behavioral and psychological symptoms in dementia; legal issues; and counseling and support for caregivers. This research team revised all the available data and compared them with the European Federation of Neurological Societies (EFNS) guideline. Further data are illustrated in Table 1, which exemplify good practice from the Department of Neurology in the University Hospital in Hradec Králové, Czech Republic. Points represent the assessment of particular medical examination or treatment according to the Act No 324/2014 Coll.8
Average costs per patient in the outpatient care
Test for tau protein may be used as a supplemental test to help with the establishment of a diagnosis of Alzheimer’s disease. Moreover, its results can distinguish between Alzheimer’s disease and other forms of dementia. These tests are not widely used or routinely ordered. Their use is limited to those suspected of dementia, and testing is typically performed after other causes of a person’s symptoms have been ruled out.
Visits to a neurologist may be two times or three–four times per year according to the patient’s condition. For the calculation of costs, a model example was used. It includes two visits to a neurologist per year, blood tests twice per year, sampling of CSF once per year, H-tau test once per year, and the cost of medication.6
A total of 2,627.52 points were required and an amount of €97 was spent (point value for 2014 was €0.037). This needs to include the cost of drugs, which is €1,745 per year.6 The average annual cost of outpatient treatment per patient was €1,842 per year. The situation of the patients examined with DG G30, G30.0, and G30.1 in the University Hospital of Hradec Králové is described in the Table 2.
Total number of patients examined with ICD Alzheimer’s Disease codes (DG G30, G30.0, and G30.1) in the University Hospital of Hradec Králové
Inpatient care and its costs
A total of 8,669 cases with primary diagnosis F01, F03, and G30 (dementia) were hospitalized in psychiatric inpatient facilities. Regarding Alzheimer’s disease, the most commonly hospitalized cases were with the diagnosis G30.1, Alzheimer’s disease with late onset (more than 38%, 1,468 cases). Between 2008 and 2012, the total number of hospitalizations of patients with dementia increased by almost a fifth (from 7,363 to 8,669). The largest increase was for Alzheimer’s disease (by almost 44%, ie, 1,170 hospitalizations).2
The number of hospitalizations for Alzheimer’s disease with late onset (DG G30.1) increased by 37% (ie, 393), and it increased by 29% (from 765 to 990 hospitalizations) for Alzheimer’s disease unspecified (DG G30.9). The number of hospitalizations of patients with Alzheimer’s disease with early onset (DG G30.0) increased only minimally in the reporting period.2 The longest treatment time on average in the reporting period was reported for Alzheimer’s disease (90 days), including Alzheimer’s disease with late onset with more than 112 days and Alzheimer’s disease with early onset with 97 days.2
In 2012, a total of 8,669 patients with dementia, ie, with basic diagnosis of F01, F03 and G30, were hospitalized in inpatient care facilities. The proportion of hospitalizations of patients with diagnosis of F01, vascular dementia, was 36% (3,129 hospitalizations) and diagnosis of G30, Alzheimer’s disease, was 44% (3,815 hospitalizations); one-fifth of the hospitalizations was linked with the diagnosis of F03, unspecified dementia (1,725 hospitalizations).2,9Table 3 describes costs for inpatient care from 2010 to 2014 in the Czech Republic.
Overview of costs for inpatient care from 2010 to 2014
Table 4 illustrates the overall number of patients with a particular diagnosis and also the cost required for treatment. It is obvious that if the disease is diagnosed earlier (G30.0), the cost is nearly two times lower than that in the later stage (G30.1). This fact supports the initial assumption of the author’s team. The implication is evident. First, the public health institutions can use this information for the purpose of prevention support and also for motivating endangered groups of people to visit doctors regularly. Moreover, the government might be interested in these outcomes and allocate financial resources more appropriately.
Overview of the costs per patient from 2010 to 2014
Health care is provided to people with dementia in the form of outpatient and inpatient care. In 2012, approximately 37,000 patients were treated in psychiatric outpatient facilities; other care (not covered by statistics) was provided in neurological and geriatric clinics. In the case of inpatient care, over 8,500 hospitalizations of people with dementia were recorded, and the average length of treatment was 78 days. People with dementia were most frequently hospitalized in psychiatric institutions and hospitals. The number of hospitalizations of people with dementia slightly increased in the last 5 monitored years by a few percent, in line with the declining average length of treatment. In case of hospitalized patients, the number of hospitalizations is monitored as a patient may be hospitalized more than once during the reporting period. Therefore, the number of hospitalized people and the number of hospitalizations vary. The comparison of the provided care in terms of sex is relevant as well. Two-thirds (65%) of hospitalized patients in outpatient care are women; in inpatient care it is 64%. When standardizing the data with the number of people of the given sex in these age groups, the differences among the sexes are not significant.9
Standardized data indicate that approximately a quarter (26%) of people with dementia use outpatient health care and less than 6% use inpatient care. The investigation showed that the underpinning of patients with Alzheimer’s disease at early onset is advantageous from an economic perspective because the cost of outpatient care is much lower compared with inpatient care. Furthermore, after discharge from hospital, the patient is usually transported to a facility for follow-up care, eg, departments for long-term patients. Family care is usually impossible due to high demands on provided services.10 In the regions of the Czech Republic, there are fundamental differences that deserve a more detailed investigation. The amount of care needed for patients with dementia is lowest in the Liberec Region and South Bohemian Region, and highest in the Moravian-Silesian Region. The amount of people with dementia who are provided with health services differ significantly among regions. In the case of inpatient care the amounts are twice as high, whereas in the case of outpatient care these are sometimes three times greater. In the regions, it is not possible to trace important context and relationships among various types of services. Therefore, it cannot be stated that one form of service is offset by another.11
The conducted research and the performed analysis are linked with a particular extent of inaccuracy, because of the lack of the public and nonpublic data. Therefore, expert estimates are used. This fact should be taken into consideration, which might be a challenge for further research.