Zhongjie HU，Jinhui WANG，Yue LANG，Xiaoling ZHAO，Jianping JIA，Ying HAN*

·Research Article·

ComParison of the neuroPsychological characteristics of two subtyPes of mild cognitive imPairment

Zhongjie HU1，Jinhui WANG2，Yue LANG3，Xiaoling ZHAO1，Jianping JIA1，Ying HAN1*

Background：Characterizing the differences between two proposed subtypes of mild cognitive impairment(MCI)—amnestic mild cognitive impairment(aMCI)and mild cognitive impairment due to small vessel disease(sv-MCI)—may help in the effort to prevent progression of MCI to Alzheimer’s dementia and vascular dementia.

Obiective：Identify neuropsychological characteristics that discriminate aMCI and sv-MCI.

Methods：50 individuals with aMCI based on Petersen’s criteria and 65 individuals with sv-MCI based on Hachinski’s criteria were identified from a general hospital neurology clinic and from a household survey in a rural district in Beijing.These subjects and 49 community members 55 and older without any cognitive problems were administered the Mini Mental State Examination(MMSE)，the Clock Drawing Test(CDT)and the Auditory Verbal Learning Test(AVLT)which assesses immediate recall，delayed recall and delayed recognition.Mean scores of these measures in the three groups of subjects were compared using a one-way analysis of variance(ANOVA) and，if significant，follow-up pairwise comparisons using Tukey tests.

Results：Mean scores on all five measures were significantly lower in the two patient groups than in the control group，and the mean subscale scores of the AVLT—immediate recall，delayed recall and delayed recognition—were significantly lower in the aMCI group than in the sv-MCI group，a difference that remained significant after adjusting for age，gender and years of education.

Conclusion：These results support previous findings of significantly greater disruption in memory functions among aMCI patients than in sv-MCI patients.Measures of memory functioning，particularly the AVLT，may be useful in distinguishing these two subtypes of MCI.

Amnesic mild cognitive impairment;Mild cognitive impairment associated with small vessel disease; Mild cognitive impairment

1 Introduction

Recently，there has been increasing interest in the entity known as mild cognitive impairment (MCI)，a condition that is often a transition state between intact memory function and dementia.A recent systematic review［1］（that included studies with subjects 60 and older，65 and older and 75 and older)reports incidence rates for MCI of 51 to 77 per 1 000 person-years.This review also subclassifies MCI into amnestic MCI(aMCI)defined as objective impairment in memory with or without impairment in other cognitive domains(which has an incidence of 9.9 to 40.6 per 1 000 personyears)and non-amnestic MCI defined as objective impairment in one of more cognitive domains other than memory(which has an incidence of 28 to 36.3 per 1 000 person-years).Amnestic MCI，which accounts for about 48%of all MCI［2］，often progresses into Alzheimer’s dementia(AD)with atrophy of the brain，especially in the mesial temporal lobes［3，4］.MCI associated with small vessel disease(sv-MCI)is one subtype of non-amnestic MCI that accounts for about 21%of all MCI［2］;it is also characterized by a relatively insidious onset and gradual cognitive deterioration that mimics aMCI. The similar patterns of cognitive decline make it difficult to differentiate sv-MCI and aMCI，particularly in the early phases of the condition［2］.Early detection of sv-MCI and differentiation from aMCI may provide an opportunity to delay cognitivedeterioration［5］and to mitigate other adverse outcomes［2］associated with sv-MCI.Moreover，as new treatments for AD are developed early identification of aMCI and differentiation from sv-MCI becomes more critical［5］.

There is no effective clinical method for differentiating aMCI and sv-MCI.Previous research examining differences between the two MCI subtypes had contradictory results［5-7］.We believe that there are measurable differences in psychological parameters that can distinguish these two conditions;the current study aims to test this hypothesis by comparing the neuropsychological characteristics of aMCI and sv-MCI.

2 Subiects and Methods

2.1 Subiect recruitment Process

The enrollment process is shown in Figure 1. Subjects were recruited from the neurology clinic at Xuanwu Hospital，Capital Medical University from September 2009 to April 2011 and from a community survey of elder adults in a rural district of Beijing conducted from September 2009 to December 2010.A semi-structured screening interview with the subject and a family member obtained basic demographic and medical history data;this was followed by a general medical and a detailed neurological examination.Subjects with scores greater than 0.5 on the Clinical Dementia Rating Scale (CDR)［8］were excluded since they were more cognitively impaired than patients with MCI.Subjects who had moderate to severe decrements in their functioning as assessed by the Activities of Daily Living Scale(ADL)［9］（ADL score≤22 for persons 75 or younger and≤24 for persons over 75)or who had moderate to severe depressive symptoms as assessed by the Hamilton Depression Rating scales(HAM-D)［10］（total score＞17)were also excluded.Other exclusion criteria included：1) cognitive impairments due psychiatric，non-MCI neurological disorders，systemic disease，alcohol or drug abuse，and so forth;and 2)visual abnormalities，severe aphasia or motor disorders that would impair the neuropsychological testing process.

Figure 1.Flowchart of the study

2.2 Classification of MCI tyPe

The Hachinski Ischemic Scale(HIS)［11］was used to identify MCI subjects with the sv-MCI subtype.The signs of cognitive impairment due to subcortical small vessel disease assessed by the HIS［5，12-15］include minor neurological signs(e.g.，hemiparesis，lower facial weakness，Babinski’s sign，sensory deficit，dysarthria，gait disorder，urine urgency，or motor slowness)and signs of moderate white matter changes(e.g.，at least one region score＞2 according to the Wahlund rating scale［16］)or two or more lacunar infarcts seen on MRI(magnetic resonance imaging)brain imaging studies.Subjects with a score of 5 or more on the HIS are considered to have the sv-MCI subtype of MCI unless they have large(＞15 mm diameter) subcortical infarcts or infarcts involving the cerebral cortex.

The Petersen’s modified criteria were used to identify subjects with the aMCI subtype of MCI［3，14，17-19］.The criteria include complaints of memory problems that persist for at least three months by the individual or a family member，objective evidence confirming the memory impairment，and no(or very mild)white matter changes or brain infarctions on brain imaging studies.

Based on these criteria 300 of the 1000 patients screened in the neurology clinic and 59 of the 400 subjects screened in the community meet criteria for MCI;these 351 MCI patients included 50 (14.2%)with aMCI，65(18.5%)with sv-MCI and 236(67.2%)with other types of MCI.Control subjects were 49 individuals from the community≥55 years of age who did not meet criteria for MCI (i.e.，community members with a CDR score of 0 and no limitations in their activities of daily living) and did not have any of the exclusion criteria.

All subjects signed written informed consent. The study protocol was approved by the Ethics Review Board of the Xuanwu Hospital.

2.3 Utilized memory instruments

The following instruments were used to assess the neuropsychological characteristics of the subjects：

2.3.1 The World Health Organization-University of California-Los Angeles Auditory Verbal Learning Test，WHO-UCLA AVLT(AVLT）［9]

This instrument is a list-learning task that assessed immediate recall，delayed recall，and delayed recognition.The Chinese version of the test has acceptable reliability and validity［20］.All 15 items in the Chinese version use one-character or two-character Chinese names of objects familiar to residents of China.They include parts of the body， tools，household objects，and common transportation vehicles.The tester reads all 15 words，one syllable every second，then asks the subject to recall as many words as possible for two minutes. This process is repeated three times(using the same words)and the three separate scores are combined;a total score of 18 words or lower(out of a potential maximum score of 45)or an average score of less than 6 on the three tests is considered abnormal.After a 20-minute interval，subjects are asked to recall the words that were read previously;six words or less is regarded as abnormal delayed recall.Finally，the tester reads a list of 30 words that includes the 15 in the original list;if the subject recognizes eight words or less this is considered abnormal delayed recognition.

2.3.2 The Clock Drawing Test(CDT）［21]

This measure is widely used to measure executive function.Subjects are asked to draw a clock with all 12 numbers and the time reading 11：10. Each step counts as one point.Three points are given for a perfect clock.The Chinese version of the test has been shown to discriminate mild cognitive impairment and mild dementia［22］.

2.3.3 Mini Mental Status Exam(MMSE）［23]

We used the MMSE to get a broad impression of the subject’s mental status.The Chinese version of the MMSE has been use extensively in China and has good psychometric properties［24，25］.The items assess orientation to time，orientation to place，computational skills(subtracting 7 from 100 three times)，short-term and delayed memory(after 1 minute)of three names，naming of objects，following of verbal and written commands，and visuospatial skills.

Researchers who administered the tests did not know the patients’diagnoses.

2.4 Statistical analysis

Data were analyzed using version 18.0 of the SPSS statistical software.We examined differences in demographic characteristics and neuropsychological test results between the aMCI，sv-MCI and control groups by one-way ANOVA analysis.If a significant between-group difference was observed，follow-up pair-wise comparisons were conducted using Tukey tests.A second one-way ANOVA analysis on the neuropsychological test scores adjusted for the potential confounding effect of age，gender，and education levels by including these variables as covariates in the analysis.

3 Results

As shown in Table 1，there were no statistically significant differences in the age，years of educationor gender between normal controls and individuals categorized as the aMCI or sv-MCI subtypes of MCI.As shown in Table 2，the mean scores of the MMSE，CDT，and the three memory subscales of the AVLT were significantly lower in the two patient groups than in the control group.For three of the measures—immediate recall，delayed recall and delayed recognition of the AVLT—the mean scores were lower in the aMCI group than in the sv-MCI group.

To exclude the potential confounding effect of age，gender and years of education on the comparison of neuropsychological test scores between the three groups，age，gender and years of education were entered as covariates in the ANOVA model. In this analysis educational level had a significant positive association with MMSE and CDT scores but the means scores on these two tests in the patient groups remained significantly lower than in the control group.None of the covariates were significantly associated with the AVLT subscale scores and the differences reported above for the unadjusted analysis remained：that is，both patient groups had significantly more severe decrements in memory functions than the control group and the impairments in the aMCI group were significantly greater than in the sv-MCI group.

Table 1.DemograPhic characteristics of aMCI，SV-MCI and NC grouPs

Table 2.Mean(SD)scores of the neuroPsychological tests in the three grouPs

4 Discussion

4.1 Main findings

This study compared the results on a variety of neuropsychological tests of control subject with those in individuals with aMCI or sv-MCI.The results confirm that aMCI and sv-MCI patients have significantly poorer cognitive functioning than normal controls and found that individuals with aMCI are more impaired than those with sv-MCI，particularly in verbal memory functioning.

Some researchers suggest that the pattern of neural disruptions of vascular dementia(VaD)(the final outcome in many individuals with sv-MCI)is primarily a"frontal-subcortical pattern"［26］，whereas the pattern of neural disruptions in Alzheimer’s dementia(AD)(the final outcome in many individuals with aMCI)is primarily a"temporal-neocortical pattern"［27］.But other research report few differences in the pattern of cognitive disruption between AD and VaD［28］.A common mechanism seen in impaired executive functioning is dysfunction in the frontal-subcortical circuits，so if VaD primarily affects frontal-subcortical regions it would be reasonable to expect that individuals with sv-MCI would have relatively more severe decrements in executive functioning compared to those with other types of MCI.Some previous studies havefound that individuals with sv-MCI have deficiencies in their executive functioning［12，29，30］but the current study did not find significant differences in executive functioning—as assessed by the Clock Drawing Test—between patients with aMCI and sv-MCI.There are several possible explanations for this negative finding that need to be clarified in subsequent research：1)there really is no difference in the regionality of the disruptions of VaD and AD;2)the CDT is not sensitive enough to identify important differences in executive function ing［31］;3)the sample size was too small to identify significant differences(the assessed power for this comparison was 94%so this is unlikely);4)the white matter lesions in the sv-MCI subjects were too small to greatly affect executive functioning; and 5)deteriorating executive functioning primarily happens in the later stages of sv-MCI as it is progressing into VaD［32］.

When using the AVLT—which specifically assesses different aspects of memory functioning—we found significantly greater dysfunction in immediate recall，delayed recall and delayed recognition in the aMCI group than in the sv-MCI group.This result is consistent with previous research［33］which also concluded that MCI subjects with aMCI were more severely impaired in verbal memory than those with sv-MCI.These results are also consistent with neuroimaging and basic anatomical research examining the brain structures important in memory.AD patients show medial temporal lobe atrophy，an area thought to be intimately involved in episodic memory function［34］.Such pathological changes have also been found in aMCI patients［35］. On the other hand，sv-MCI patients have different degrees of diffuse white matter changes and medial temporal lobe atrophy，affecting the frontal-sub-cortical circuits and，thus，having a less pronounced effect on memory.

Previous research has also indicated that deficits in the prefrontal cortex and the medial temporal lobe have different roles in memory function［36］.The left temporal lobe is thought to be crucial for information storage［37］while the left frontal cortex is involved both in retrieval of memories［38］and in working memory［39］.It is，therefore，reasonable to expect that the different neuropathological changes in aMCI and sv-MCI would result in different patterns of memory deficits that could be discriminated by neuropsychological testing.

4.2 Limitations

Several limitations need to be taken into consideration when interpreting these results.1) The study subjects came from one hospital and one rural community so it’s uncertain how representative they are of individuals with MCI from other locations.2)The MCI cases included in the study combined those identified in the community and in a neurological outpatient clinic so its hard to specify the sampling frame for the cases.3)The high proportion of all individuals with MCI classified as‘other subtypes of MCI’(67%)was unexpected; either previous reports about the proportion of the different subtypes of MCI are incorrect or there was something specific about our classification algorithm that excluded most of the MCI cases.4)The CDT and MMSE tests are general measures of cognition，they did not provide detailed assessment of executive functioning or of the other components of cognition.

4.3 ImPlications

We have found that several types of memory functioning are significantly more impaired in aMCI than in sv-MCI，even after adjusting for gender，age and level of education.Subsequent studies with larger and more diverse samples are needed to confirm these findings but they suggest that relatively simple tests of memory functioning—such as the Auditory Verbal Learning Test—can help to discriminate aMCI from sv-MCI.Additional studies will also be needed to identify the cut-off points for the memory scales with the best sensitivity and specificity compared to a gold-standard diagnosis(i. e.，using brain imaging).The resulting relatively simple memory test could be used to screen highrisk individuals to identify those who need more detailed assessment to determine the definitive diagnosis.Given the different clinical course and treatments for AD and VaD，discriminating common pre-cursor conditions for these disorders like aMCI and sv-MCI could have substantial clinical benefits，particularly in settings where it is not possible to conduct brain scans.

Conflict of Interest

The authors report no conflict of interest.

Funding

This work was supported by National Natural Science Foundation of China(grants 30970823 and 30830045).

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·論著·

兩種輕度認知損害患者的神經(jīng)心理學(xué)功能比較

胡忠婕1王金輝2朗 悅3趙筱玲1賈建平1韓 瓔1

國家自然科學(xué)基金面上資助項目（30970823）；國家自然科學(xué)基金重點項目（30830045）

1首都醫(yī)科大學(xué)宣武醫(yī)院神經(jīng)內(nèi)科100053；2北京師范大學(xué)認知神經(jīng)科學(xué)與學(xué)習(xí)國家重點實驗室100089；3大連醫(yī)科大學(xué)附屬第二醫(yī)院癲癇中心116023。通信作者：韓瓔，電子信箱sophiehanying@gmail.com

背景區(qū)別輕度認知損害（mild cognitive impairment,MCI）的兩種亞型，即遺忘型輕度認知損害（amnestic mild cognitive impairment,aMCI）和小血管型輕度認知損害（MCI associated with small vessel diseases,sv-MCI）將有利于延緩和預(yù)防MCI進展為阿爾茨海默病性癡呆和血管性癡呆。

目的識別并區(qū)分區(qū)aMCI與sv-MCI的神經(jīng)心理學(xué)特征。

方法從宣武醫(yī)院神經(jīng)科門診就診患者或在北京社區(qū)進行的一項入戶調(diào)查中選擇符合入組標(biāo)準(zhǔn)的被試。根據(jù)Petersen診斷標(biāo)準(zhǔn)篩選aMCI患者50例，根據(jù)Hachinski診斷標(biāo)準(zhǔn)篩選sv-MCI患者65例。以上兩組患者和49名55歲以上沒有認知障礙的社區(qū)被試一同接受簡明精神狀態(tài)量表（Mini Mental State Examination,MMSE）檢查及畫鐘測驗（Clock Drawing Test,CDT）與聽覺詞語學(xué)習(xí)測驗（Auditory Verbal Learning Test,AVLT,評定即刻記憶、延遲回憶和延遲再認能力）。采用單因素方差分析法比較3組被試各項測驗的平均得分，如果結(jié)果存在明顯差異，再進行多個樣本兩兩比較的Tukey法檢驗。

結(jié)果aMCI組和sv-MCI組5項測驗平均得分均明顯低于健康對照組。aMCI組AVLT即刻記憶、延遲回憶和延遲再認測驗得分均低于sv-MCI組。在校正了年齡、性別、受教育年限后，上述差異仍舊存在。

結(jié)論實驗結(jié)果與既往結(jié)果一致，與sv-MCI患者相比，aMCI患者記憶損害更加明顯。記憶相關(guān)的評估測驗，尤其是AVLT,或?qū)⒂兄趨^(qū)別這兩種MCI亞型。

遺忘型輕度認知損害 小血管型輕度認知損害 輕度認知損害

10.3969/j.issn.1002-0829.2011.05.002

1Department of Neurology，Xuanwu Hospital，Capital Medical University，Beijing，100053 China

2State Key Lab of Cognitive Neuroscience and Learning，Beijing Normal University，Beijing，100089 China3Epilepsy Center，Second Affiliated Hospital of Dalian Medical University，116023 China

*Correspondence：sophiehanying@gmail.com