Archives of Gerontology and Geriatrics

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1 Archives of Gerontology and Geriatrics 49 (2009) Contents lists available at ScienceDirect Archives of Gerontology and Geriatrics journal homepage: Effects of spaced retrieval training (SRT) on cognitive function in Alzheimer s disease (AD) patients Seok Bum Lee a, Chong Soon Park b, Ji Woon Jeong b, Jin Young Choe b, Yun Jung Hwang b, Chung-A Park b, Joon Hyuk Park b, Dong Young Lee c, Jin Hyeong Jhoo d, Ki Woong Kim b,c, * a Department of Psychiatry, Dankook University Hospital, 16-5 Anseodong, Cheonan, Chungcheongnamdo , Republic of Korea b Department of Neuropsychiatry, Seoul National University Bundang Hospital, 300 Gumidong, Bundanggu, Seongnam, Gyeonggido , Republic of Korea c Department of Psychiatry, Seoul National University College of Medicine, 28 Yeongeondong, Jongnogu, Seoul , Republic of Korea d Department of Neuropsychiatry, Kangwon National University Hosptial, 26 Kangwondaehakro, Chuncheon, Kangwondo , Republic of Korea ARTICLE INFO ABSTRACT Article history: Received 16 June 2008 Received in revised form 27 October 2008 Accepted 29 October 2008 Available online 18 December 2008 Keywords: Spaced retrieval training Alzheimer s disease Memory improvement Among the non-pharmacological treatments of dementia, SRT is a good candidate strategy for rehabilitating the cognition of AD patients. This study investigates the efficacy of SRT on the cognition of AD patients with very mild to mild disease. We administered 24-session SRT to 13 very mild and 6 mild AD patients. To assess the change of the neuropsychological performance after SRT, we performed the Korean version of the Consortium to Establish a Registry for Alzheimer s Disease neuropsychological battery (CERAD-K), the logical memory test (LMT), the Benton visual retention test A (BVRT-A), and the digit span test (DST). All tests were administered both before and after SRT. Retention spans were significantly increased up to 24 min after SRT in both very mild and mild AD patients (p < 0.05), and this improvement was maintained for different sets of target information. Retainable words were also significantly increased after SRT in the very mild AD patients (p = 0.007). However, we observed no changes in neuropsychological performance after SRT. Although we did not observe improvements in the neuropsychological tests following SRT, our results suggest that the treatment was an effective intervention for improving the memory of very mild to mild AD patients, and could potentially improve learning and retention outside the training session. ß 2008 Elsevier Ireland Ltd. All rights reserved. 1. Introduction AD is one of the most distressing and burdensome mental health problems in the aged population. Although acetylcholinesterase inhibitors (e.g., tacrine, donepezil, rivastigmine, and galantamine) and N-methyl-D-aspartate (NMDA) receptor antagonists (e.g., memantin) have demonstrated efficacy in the temporal symptomatic control of cognitive decline and daily function in AD patients, their effect is not good enough to restore premorbid function, nor is it maintained in the later stages of AD (O Hara et al., 2000). Therefore, a multi-factorial therapeutic approach that includes both pharmacological and non-pharmacological interventions is being increasingly advocated in order to optimize the cognition, affect and global functioning of AD patients (Newhouse et al., 1997). Non-pharmacological treatments of persons with * Corresponding author at: Department of Neuropsychiatry, Seoul National University Bundang Hospital, 300 Gumidong, Bundanggu, Seongnam, Gyeonggido , Republic of Korea. Tel.: ; fax: address: kwkimmd@snu.ac.kr (K.W. Kim). dementia differ from pharmacological treatments in that they consider the interaction between the patient and therapist, and are personalized to consider the needs and performance of the patient. This sort of treatment has been shown to temporarily slow the rate of overall cognitive decline and loss of functional abilities while reinforcing a positive sense of self (Yesavage et al., 1981; De Vreese and Neri, 1999). Since the cognitive decline is the earliest core symptom in AD and the available cognitive enhancers have only limited efficacy, cognitive rehabilitation is a critical part of the nonpharmacological treatments for AD (O Hara et al., 2000). However, many of the cognitive rehabilitation techniques that have proven beneficial for non-demented older individuals with age-related memory loss have failed in AD patients because they require considerable amounts of cognitive effort and episodic memory, both of which begin to deteriorate in the early stages of AD (Backman, 1992, 1996). In this sense, SRT is a good candidate strategy for rehabilitating the cognition of AD patients because it does not require much cognitive effort. SRT, a method of learning and retaining target information by recalling that information over increasingly longer intervals (Camp, 1989), was developed on the basis of the /$ see front matter ß 2008 Elsevier Ireland Ltd. All rights reserved. doi: /j.archger

2 290 S.B. Lee et al. / Archives of Gerontology and Geriatrics 49 (2009) expanding rehearsal technique they had originally developed for improving memory in cognitively intact persons (Camp and Stevens, 1990; Camp et al., 1996). The modification was designed to reduce the learner s effort during training, reduce the number of errors by matching the difficulty of the task to the patient s ongoing performance (shaping paradigm), and make the training sessions social and enjoyable (Camp and Stevens, 1990). SRT has been reported to improve learning and target information retention, and to ameliorate behavioral problems in various types of dementia, including AD (Camp and Stevens, 1990; Abraham and Camp, 1993; Bird et al., 1995; Bird, 1998, 2001; Cherry and Simmons-D Gerolamo, 2005). However, the previous studies suffered from several methodological limitations. First, the retrieval spans used in training sessions during most of the previous studies were short (less than 10 min), meaning that they did not directly examine the effect of SRT on the long-term retention of target information (McKitrick et al., 1992; Cherry et al., 1999; Cherry and Simmons-D Gerolamo, 2005). Second, the previous studies did not sufficiently investigate whether the effect of SRT on remembering target information could be transferred to targets other than the training materials. In one previous study (Hawley and Cherry, 2004), AD patients were trained by an SRT in which the participants were shown a target photograph and stated the name of the individual in that photograph at increasingly longer retention intervals. Notably, these patients were additionally able to call the live person by the correct name. However, although this result provided initial evidence that SRT of face name association might transfer to a live person, the results did not allow for statistical analysis. Moreover, strictly speaking, an actual person and his/her photograph should not be considered different pieces of information. Third, the influence of SRT on neuropsychological performance was not comprehensively investigated in the previous studies (McKitrick et al., 1992; Cherry and Simmons- D Gerolamo, 2005; Hochhalter et al., 2005), with the one exception of the report by Davis et al. (2001). Fourth, comorbid reversible cognitive declines such as those associated with depression or metabolic disorders might have confounded the previous results, since the performed diagnostic evaluations were not structured or extensive. Therefore, we designed the present study to investigate the effect of SRT on the cognition of patients with very mild to mild AD, while overcoming the limitations of the prior studies in the following ways. First, our SRT program consisted of 24 sessions that were given regularly every other day for 8 weeks, and the maximum retrieval interval was set at 24 min in order to examine the effect of SRT on long-term retention of target information. Second, different word sets were used in each session, in order to evaluate whether the effect of SRT could be transferred to the learning of other information. Third, we administered comprehensive neuropsychological tests to investigate whether they could reflect the effect of SRT. Fourth, all standardized clinical interviews, neurological and physical examinations were conducted by geriatric psychiatrists with advanced training in neuropsychiatry and dementia research. 2. Subjects and methods 2.1. Subjects Study participants were enrolled from among visitors to the dementia clinic of the Seoul National University Bundang Hospital. The CERAD-K (Lee et al., 2002) was administered to each subject, and his/her diagnosis and Clinical Dementia Rating (CDR) were determined at a consensus committee meeting. The diagnosis of dementia was made according to the DSM-IV criteria (APA, 1994), and the diagnosis of AD was made according to the criteria of the National Institute of Neurological and Communicative Disorders and Stroke and the Alzheimer s Disease and Related disorder Association (NINCDS ADRDA) (McKhann et al., 1984). The AD patients were stratified into two severity groups: those with a CDR of 0.5 were enrolled in the very mild AD group, and those with a CDR of 1 were enrolled in the mild AD group. Patients with a CDR of 2 or higher were excluded. Each participant s retention span and the maximum number of retainable words was estimated before SRT and used as the baseline measurement. In this measurement, each subject was asked to remember a given set of words and then to recall them immediately. If the subject succeeded in recalling them, he/she was asked to recall them repeatedly over systematically expanded intervals (1.5, 3, 6, 12 and 24 min). The set of words consisted of one to five unrelated high-imagery words (e.g., butterfly ). All words were disyllabic words in the Korean language. If the subject failed to remember the five-word set for 1.5 min, the test was repeated with the number of words in the set being sequentially reduced to one. AD patients whose CDR was 2 or higher, and those who could not retain one word for more than 1.5 min in the baseline test were excluded since we assumed that they might not have the minimum ability required to benefit from SRT (Brush and Camp, 1998). Subjects who were diagnosed as having Axis I disorders, including major depressive disorder, by DSM-IV criteria (APA, 1994) and those who had serious medical and neurological disorders that could affect their mental function were also excluded. The study protocol was approved by the Institutional Review Board of the Seoul National University Bundang Hospital. Informed consent was obtained for each subject, either directly or from his/ her guardian Assessments To assess changes in neuropsychological performance after SRT, we performed the Korean version of the CERAD neuropsychological battery (Lee et al., 2002), the LMT (Wechsler, 1987), the BVRT- A(Sivan, 1992), and the DST (Wechsler, 1987). We also assessed depressive symptoms using the Korean version of the Geriatric Depression Scale (GDS-K) (Bae and Cho, 2004). All assessments were performed before and after SRT. The intervals between SRT and pre-/post-assessments did not exceed 2 weeks Procedure A total of 24 SRT sessions were given to each participant, every other day for 8 weeks. In each SRT session, the subject was asked to remember a given set of words and then recall them immediately. If the subject succeeded in recalling the words, he/she was asked to recall them repeatedly over systematically expanded intervals (1.5, 3, 6, 12 and 24 min). Following a recall failure, the interval was reduced to that of the previous trial. The set of words consisted of one to five unrelated high-imagery words (e.g., bus, grape, duck, scissors, etc.). All targets were disyllabic words in the Korean language, and different words were used in all sessions, including the baseline measurement. The number of words in the first session was set at the number of words that the given subject had succeeded in recalling at 1.5 min in the baseline measurement. If the subject succeeded in recalling the given set of words for 24 min in two sessions, the number of words in the set was sequentially increased in the subsequent session. During each interval, the subject was asked to perform inter-retrieval activities in order to prevent him/her from rehearsing the given set of words. The interretrieval activities consisted of enjoyable activities that did not

3 S.B. Lee et al. / Archives of Gerontology and Geriatrics 49 (2009) require much memory function, but could improve fine motor, attention, and problem solving (e.g., putty, jenga, halli-galli, etc.) Statistical analysis The Mann Whitney U-test was used to compare demographic characteristics, neuropsychological performances, and GDS-K scores between the very mild and mild AD groups. The Wilcoxon signed ranks test was used to compare pre- and post-srt performance, neuropsychological performance and depressive symptoms. All statistical analyses were performed using SPSS version Results Thirty-one AD patients (7 men, 24 women) were initially enrolled, 19 of whom (1 man, 18 women) completed the present study. The proportion of men was higher in the drop-out group than in the completion group (p = 0.007, Fisher s exact test). However, there was no significant difference in age (p = 0.935, Mann Whitney U-test), education (p = 0.806, Mann Whitney U- test), the Korean version of Mini-Mental State Examination (MMSE-KC) (Lee et al., 2002) scores (p = 0.463, Mann Whitney U-test), or CDR (p = 0.705, Fisher s exact test) between the two groups. Thirteen of the subjects who completed the present study were diagnosed with very mild AD (CDR = 0.5) and the other six were diagnosed with mild AD (CDR = 1) (Table 1). There were no differences in the mean ages and education levels between the very mild AD and mild AD groups (p > 0.05, Mann Whitney U-test). Sixteen subjects were taking acetylcholine esterase inhibitors at the time of the study. Among them, 14 were taking donepezil (mean dose = 8.6 mg) and the other two were taking galantamine (mean dose = 14 mg). The mean duration of medication use was 10.4 months by the end of the SRT. The remaining three patients were not taking any cognitive enhancers at the time of the study, due to low economic status. Table 2 shows the changes of retention time and the number of words retained for at least 1.5 min over the course of the study. The Table 1 Demographic characteristics of the subjects (mean S.D.). Number of patients Age (years) Sex (% female) Education (years) MMSE-KC * GDS-K * p = 0.048, Mann Whitney U-test. retention time for a given number of words was significantly increased after SRT in both the very mild AD group (pre- SRT = , post-srt = , p = 0.002, Wilcoxon signed ranks test) and the mild AD group (pre-srt = , post- SRT = , p = 0.043, Wilcoxon signed ranks test). The number of words retained for at least 1.5 min was also higher after SRT; this change was statistically significant in the very mild AD group (pre- SRT = , post-srt = , p = 0.007, Wilcoxon signed ranks test). As shown in Table 3, we did not observe significant improvements in neuropsychological test performance. There was some improvement in performance of BNT, which measures the ability to retrieve semantic memory, but this change did not reach the level of statistical significance (pre-srt = , post- SRT = , p = 0.063, Wilcoxon signed ranks test). 4. Discussion The present study was designed to examine whether SRT is applicable as a cognitive rehabilitation technique for AD patients in clinical settings, while overcoming several methodological limitations of the previous studies on SRT. We improved upon the previous studies in four major ways. First, we extended the in-session maximum retention span to 24 min, in order to evaluate whether the retention of target information is long enough to be helpful in forming long-term memory. It has been suggested that SRT may increase the retention span of target information by repetition priming (McKitrick et al., 1992; Cherry and Simmons-D Gerolamo, 2005), a non-conscious form of memory that is accompanied by reductions in neural activity when an experience is repeated. Compared with explicit memory, repetition priming is relatively impervious to the effects of age (Wiggs et al., 2006), and its effect can last more than a month (Wiggs et al., 2006). This study showed that SRT could increase the retention span up to 24 min in patients with very mild and mild AD. This duration is much longer than that examined in previous studies (McKitrick et al., 1992; Cherry et al., 1999; Cherry and Simmons-D Gerolamo, 2005), and suggests that SRT may be helpful for improving the storage of target information in the everyday lives of AD patients. Second, by changing the target information used in each training session, we demonstrated that the SRT-induced improvements in retention span could be transferred from one target to another. Our findings are consistent with a prior study showing that the SRT effect could be transferred in a name face recognition task (Hawley and Cherry, 2004). These results indicate that SRT may be able to improve the learning and retention of AD patients outside the training session. The observed improvement of learning ability might be due to the spacing effect and/or shaping paradigm (McKitrick et al., 1992; Camp et al., 1996). The former Table 2 Changes in the retention time and number of retained words after SRT in AD patients. Pre-SRT Post-SRT Pre-SRT Post-SRT Pre-SRT Post-SRT Retention span a ** * *** Retained words b ** ** Notes: a The retention time in the baseline test administered before SRT was compared with the maximum retention time for the same number of words achieved in the SRT sessions. b The number of words retained for at least 1.5 min in the baseline test administered before SRT was compared with the maximum number of words retained for at least 1.5 min in the SRT sessions. * p < 0.05, Wilcoxon signed ranks test. ** p < 0.01, Wilcoxon signed ranks test. *** p < 0.001, Wilcoxon signed ranks test.

4 292 S.B. Lee et al. / Archives of Gerontology and Geriatrics 49 (2009) Table 3 The effects of SRT on the neuropsychological performance of AD patients (mean S.D.). MMSE-KC Pre Post Boston naming test Pre Post Word list memory test Pre Post Word list recall test Pre Post Word list recognition test Pre Post Logical memory tests (LMT) Immediate recall, story Pre Post Immediate recall, theme Pre Post Delayed recall, story Pre Post Delayed recall, theme Pre Post Recognition Pre Post BVRT-A Pre Post DST Forward Pre Post Backward Pre Post indicates that the effects of memory practice or repetition on memory improvement may be enhanced when the repetitions are separated rather than massed (McKitrick et al., 1992), while the latter links the difficulty of a task to the patient s performance (Park and Ingles, 2001), with patients performing better on target tasks if the initial task is not too demanding and the more difficult task is required successively (Ball, 1993). Moreover, by increasing the number of target words during SRT, we demonstrated that SRT may also increase the number of retainable words in a given retention span. This suggests that SRT may enhance working memory in the early stages of AD, when impairments in working memory lead to difficulties in learning new information (Kensinger et al., 2003; Germano and Kinsella, 2005). If this is the case, then SRT-induced improvements in working memory might improve the acquisition of new information in patients with AD. Third, we administered comprehensive neuropsychological tests to investigate whether they could reflect the effect of SRT. As a result, SRT did not have a significant effect on the patients performances on the global cognition test and the comprehensive verbal and visual episodic memory tests. Similar findings were reported in two previous studies (Camp et al., 1996; Davis et al., 2001). This discrepancy between the effect of SRT on retention span and retainable words and conventional neuropsychological measures may be partly attributed to differences in the cognitive efforts and explicit memory required for performing SRT and conventional neuropsychological tests. Since new learning in SRT is mainly implicit (Camp et al., 1996; Cherry et al., 1999; Cherry and Simmons-D Gerolamo, 2005), less cognitive effort and explicit memory may be required for SRT compared to conventional neuropsychological tests. In addition, due to the small sample size (N = 19), the statistical power of the present study might not have been sufficient to detect a modest change in neuropsychological performance. Fourth, we minimized the diagnostic misclassification of the subjects by using a standardized structured diagnostic interview. The elderly commonly present conditions such as depression, delirium, and metabolic disorders, all of which may cause reversible cognitive decline. Misclassification of these reversible conditions as AD may seriously confound the results of studies such as these. Although our study has a number of strengths over the previous reports, several limitations should be noted. First, for ethical reasons we allowed the subjects to take cognitive enhancers. Sixteen out of the 19 study subjects had been taking acetylcholine esterase inhibitors for 10 months or more by the end of the SRT. Although the concomitant use of medication might have confounded the apparent effect of SRT observed in this study, we argue that the medication was unlikely to have had a strong effect on our findings because the mean duration of medication was longer than 10 months, and previous studies have shown that patients treated with acetylcholine esterase inhibitors showed maximum cognitive improvements at 3 6 months, with these improvements declining slowly thereafter (Mohs et al., 2001; Pirttila et al., 2004). Second, it was not clear whether the improvement in the retention time and span should be attributed to the SRT or the enjoyable interretrieval activities. To exclude the effect of inter-retrieval activities, a future study should compare the SRT group with a control group that receives only inter-retrieval activities during the timeframe. Third, a relatively high proportion of study subjects dropped out (38.7%). This was seen especially in men (85.7% of enrolled male participants), mainly because many of the male patients regarded the utilized inter-retrieval activities as being childish. Therefore, a future study should use inter-retrieval activities that are more acceptable to male participants, allowing them to apply SRT effectively without giving up. Fourth, we did not look for the long-term effectiveness of SRT. In conclusion, we herein found that SRT was an effective intervention for improving the memory of very mild to mild AD patients. We further found evidence that SRT could improve the patients learning and retention outside the training session. Future work will be required to confirm the latter effect through a randomized mock-therapy-controlled comparison study with a larger sample size and longer follow-up duration. Acknowledgement This work was supported by Grant from Eisai Korea Inc. The sponsor was not involved in conducting the study. Conflict of interest None.

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