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Scoring systems for the Clock Drawing Test: A historical review

Sistemas de pontuação do Teste do Desenho do Relógio: Uma revisão histórica

ABSTRACT

The Clock Drawing Test (CDT) is a simple neuropsychological screening instrument that is well accepted by patients and has solid psychometric properties. Several different CDT scoring methods have been developed, but no consensus has been reached regarding which scoring method is the most accurate. This article reviews the literature on these scoring systems and the changes they have undergone over the years. Historically, different types of scoring systems emerged. Initially, the focus was on screening for dementia, and the methods were both quantitative and semi-quantitative. Later, the need for an early diagnosis called for a scoring system that can detect subtle errors, especially those related to executive function. Therefore, qualitative analyses began to be used for both differential and early diagnoses of dementia. A widely used qualitative method was proposed by Rouleau et al. (1992). Tracing the historical path of these scoring methods is important for developing additional scoring systems and furthering dementia prevention research.

Key words:
Clock Drawing Test; scoring; neuropsychology; screening test

RESUMO

O Teste do Desenho do Relógio (TDR) é um instrumento de rastreio neuropsicológico simples bem aceito pelos pacientes e com sólidas propriedades psicométricas. Em meio aos métodos de pontuação, não existe consenso com relação aos que tenham maior acurácia. Esse artigo tem como objetivo realizar uma revisão histórica sobre os sistemas de pontuação mais utilizados e as mudanças ocorridas com os mesmos ao longo dos anos. No decorrer do caminho histórico, diferentes tipos de sistemas de pontuação surgiram. Inicialmente, o foco era no rastreio de demência e os métodos utilizados eram quantitativos e semi-quantitativos. Contudo, em um segundo momento, a necessidade de diagnóstico precoce demandou o uso de um sistema de pontuação que pudesse especificar erros sutis especialmente aqueles relacionados a funções executivas. Assim, análise qualitativa começou a ser mais usada em ambos no diagnóstico diferencial e precoce de demência. Um método qualitativo amplamente utilizado é o de Rouleau et al. (1992). O caminho histórico é importante para o desenvolvimento dos sistemas de pontuação e também para as pesquisas de prevenção de demência.

Palavras-chave:
Teste do Desenho do Relógio; pontuação; neuropsicologia; teste de rastreio

INTRODUCTION

The Clock Drawing Test (CDT) is recognized worldwide as a neuropsychological screening test that has solid psychometric properties, including test-retest reliability11. Mendez MF, Ala T, Underwood KL. Development of scoring criteria for the clock drawing task in Alzheimer's disease. J Am Geriatr Soc. 1992;40:1095-9.,22. Strauss E, Sherman EMS, Spreen O. A Compendium of Neuropsychological Tests: Administration, Norms, and Commentary (3rd ed.). New York: Oxford University Press; 2006. and inter-rater reliability.33. Fuzikawa C, Lima-Costa MF, Uchoa E, Barreto SM, Shulman KI. A population based study on the intra and inter-rater reliability of the clock drawing test in Brazil: the Bambuí Health and Ageing Study. Int J Geriatr Psychiatry. 2003;18:450-6.

4. García-Caballero A, Recimil MJ, García-Lado I, Gayoso P, Cadarso-Suarez C, Gonzalez-Hermida J, et al. ACE clock scoring: a comparison with eight standard correction methods in a population of low educational level. J Geriatr Psychiatry Neurol. 2006;19:216-9.

5. Hubbard EJ, Santini V, Blankevoort CG, Volkers KM, Barrup MS, Byerly L, et al. Clock drawing performance in cognitively normal elderly. Arch Clin Neuropsychol. 2008;23:295-327.
-66. Nair AK, Gavett BE, Damman M, Dekker W, Green RC, Mandel A, et al. Clock drawing test ratings by dementia specialists: interrater reliability and diagnostic accuracy. J Neuropsychiatry Clin Neurosci. 2010;22:85-92. The CDT correlates well with other instruments, such as the Mini-Mental State Examination (MMSE), Cambridge Cognitive Examination (CAMCOG), and Rey Complex Figure Test, among others.11. Mendez MF, Ala T, Underwood KL. Development of scoring criteria for the clock drawing task in Alzheimer's disease. J Am Geriatr Soc. 1992;40:1095-9.,77. Shulman, K.I., Herrmann N, Brodaty H, Chiu H, Lawlor B, Ritchie K, et al. IPA survey of brief cognitive screening instruments. Int Psychogeriatr. 2006;18:281-94.

8. Heinik J, Solomesh I, Berkman P. Correlation between the CAMCOG, the MMSE, and three clock drawing tests in a specialized outpatient psychogeriatric service. Arch Gerontol Geriatr. 2004;38:77-84.

9. Manos PJ, Wu R. The ten point clock test: a quick screen and grading method for cognitive impairment in medical and surgical patients. Int J Psychiatry Med. 1994;24:229-44.

10. Sunderland T, Hill JL, Mellow AM, Lawlor BA, Gundersheimer J, Newhouse PA, et al. Clock drawing in Alzheimer's disease: a novel measure of dementia severity. J Am Geriatr Soc . 1989;37:725-9.

11. Rouleau I, Salmon DP, Butters N, Kennedy KC, McGuire K. Quantitative and qualitative analyses of clock drawings in Alzheimer's and Huntington's disease. Brain Cogn. 1992;18:70-87.
-1212. Freedman M, Leach L, Kaplan E, Winocur G, Shulman KI, Delis CD. Clock Drawing: a neuropsychological analysis. New York: Oxford University Press ; 1994. It is usually used to screen for cognitive decline in older adults and discriminate healthy individuals from those with dementia, especially Alzheimer's disease (AD). The CDT is well accepted by patients and widely employed as a follow-up instrument because it can be easily and quickly applied and scored.1313. Shulman KI. Clock-drawing: is it the ideal cognitive screening test? Int J Geriatr Psychiatry . 2000;15:548-61.

While drawing the clock, different cortical systems work simultaneously, including the frontal, parietal, and temporal lobes.1212. Freedman M, Leach L, Kaplan E, Winocur G, Shulman KI, Delis CD. Clock Drawing: a neuropsychological analysis. New York: Oxford University Press ; 1994.,1414. Aprahamian I. O Teste do Desenho do Relógio no rastreio diagnóstico da doença de Alzheimer em idosos no Brasil. Dissertação de Mestrado. Campinas: Faculdade de Ciências Médicas da Universidade Estadual de Campinas; 2008.,1515. Ueda H, Kitabayashi Y, Narumoto J, Nakamura K, Kita H, Kishikawa Y, Fukui K. Relationship between clock drawing test performance and regional cerebral blood flow in Alzheimer's disease: A single photon emission computed tomography study. Psychyatry Clin Neurosci. 2002;56: 25-9.Thus, different cognitive abilities can be measured, such as selective and sustained attention, auditory comprehension, verbal working memory, numerical knowledge, visual memory and reconstruction, visuospatial skills, on-demand motor execution (praxis), and executive function.11. Mendez MF, Ala T, Underwood KL. Development of scoring criteria for the clock drawing task in Alzheimer's disease. J Am Geriatr Soc. 1992;40:1095-9.

Some features influence the CDT, such as age and education. A number of authors also consider language an influential factor.1616. Pinto E, Peters R. Literature review of the Clock Drawing Test as a tool for cognitive screening. Dement Geriatr Cogn Disord. 2009;27:201-13. Older adults usually exhibit more impaired performance than young adults,1212. Freedman M, Leach L, Kaplan E, Winocur G, Shulman KI, Delis CD. Clock Drawing: a neuropsychological analysis. New York: Oxford University Press ; 1994.,1717. Gruber NP, Varner RV, Chen Y, Lesser JM. A comparison of the clock drawing test and the Pfeiffer Short Portable Mental Status Questionnaire in a geropsychiatric clinic. Int J Geriatr Psychiatr. 1997;12:526-32.

18. Crowe M, Allman RM, Triebel K, Sawyer P, Martin RC. Normative performance on an Executive Clock Drawing Task (CLOX) in a community-dwelling sample of older adults. Arch Clin Neuropsychol . 2010;25: 610-17.
-1919. Paula JJ, Miranda DM, Moraes EN, Malloy-Diniz LF. Mapping the clock works: what does the Clock Drawing Test assess in normal and pathological aging? Arq Neuropsiquiatr. 2013;71:763-8. and greater years of formal education are associated with better performance on the test.1818. Crowe M, Allman RM, Triebel K, Sawyer P, Martin RC. Normative performance on an Executive Clock Drawing Task (CLOX) in a community-dwelling sample of older adults. Arch Clin Neuropsychol . 2010;25: 610-17.

19. Paula JJ, Miranda DM, Moraes EN, Malloy-Diniz LF. Mapping the clock works: what does the Clock Drawing Test assess in normal and pathological aging? Arq Neuropsiquiatr. 2013;71:763-8.

20. Lourenço RA, Ribeiro-Filho ST, de Freitas Henriques Moreira I, Paradela EMP, Miranda AS. The Clock Drawing Test: performance among elderly with low educational level. Rev Bras Psiquiatr. 2008;30:309-15.
-2121. Royall DR. The "Alzheimerization" of dementia research. J Am Geriatr Soc . 2003;51:277-8.

Clock Drawing Test performance was originally used as an indicator of constructional apraxia. During World War II, it was employed in studies of soldiers who were victims of head trauma and had possible focal lesions in the occipital and parietal lobes. Goodglass and Kaplan2222. Goodglass H, Kaplan E. The assessment of aphasia and related disorders. Philadelphia: Lea and Febiger; 1983. conducted the first systematic study of the CDT as part of the Boston Aphasia Battery.1313. Shulman KI. Clock-drawing: is it the ideal cognitive screening test? Int J Geriatr Psychiatry . 2000;15:548-61.

Although the CDT had been mainly used to assess visuoconstructional disorders, clinical staging scales for the study of AD began to be developed in the 1980s to provide a more specific classification of intellectual performance in the geriatric population.2323. Golomb J, Kluger A, Ferris SH. Mild cognitive impairment: historical development and summary of research. Dialogues Clin Neurosci. 2004;6:351367. In August 1986, Shulman and collaborators published the first study employing the CDT as a screening tool for older adult patients with cognitive disorders.14 Since then, studies have been performed to characterize its contributions both as a screening instrument in cognitive impairment and for the diagnosis and follow-up of Huntington's disease, schizophrenia, unilateral neglect, delirium, multiple sclerosis, and other pathologies.1313. Shulman KI. Clock-drawing: is it the ideal cognitive screening test? Int J Geriatr Psychiatry . 2000;15:548-61.

Different studies have used a wide range of administration and scoring criteria, resulting in heterogeneous findings and a lack of consensus with regard to which criteria produce the best results. In this context, the need for putting together a logical timeline that better explained the development of CDT scoring systems emerged. Taking into account the large number of studies since 1986, a selection criterion based on relevance was indispensable. The articles were selected based on their importance to the development of CDT scoring systems throughout history. Therefore, the articles that met the criteria of representing a significant milestone and/or change in the development of CDT scoring systems were included. Finally, the aim of this article was to conduct a historical literature review of CDT scoring systems, describing the development and changes that have taken place throughout the years.

SCORING SYSTEMS CLASSIFICATIONS

Shulman1313. Shulman KI. Clock-drawing: is it the ideal cognitive screening test? Int J Geriatr Psychiatry . 2000;15:548-61. highlighted that no matter which method is employed, the specificity and sensitivity of the CDT depend more on the interpretation of the test than the way the test is administered. The presentation of different scoring procedures is intended to provide clinicians with as much information as possible about these procedures. However, because reviewing all of these in detail would be beyond the scope of the present study, we focus instead on the tendencies and changes that the scoring systems have undergone over the years.

Different methods of scoring the CDT emerged, and the classifications of scoring systems often diverged. For the purposes of the present study, our classifications were based on Ehreke et al.2424. Ehreke L, Luck T, Luppa M, König HH, Villringer A, Riedel-Heller SG. Clock drawing test: screening utility for mild cognitive impairment according to different scoring systems: results of the Leipzig Longitudinal Study of the Aged (LEILA 75+).Int Psychogeriatr . 2011;23:1592-601. and Patocskai et al..2525. Patocskai AT, Pakaski M, Vincze G, Fullajtar M, Szimjanovszki I, Drotos G, et al. Is there any differences between the findings of Clock Drawing Tests if the clock shows different times? J Alzheimers Dis. 2014;39:749-57. These authors considered quantitative analyses as those represented by numerical scales. Qualitative analyses classify the drawing of the clock based on descriptions of typical errors by considering the whole clock in their analysis and using a subjective approach.2424. Ehreke L, Luck T, Luppa M, König HH, Villringer A, Riedel-Heller SG. Clock drawing test: screening utility for mild cognitive impairment according to different scoring systems: results of the Leipzig Longitudinal Study of the Aged (LEILA 75+).Int Psychogeriatr . 2011;23:1592-601.,2525. Patocskai AT, Pakaski M, Vincze G, Fullajtar M, Szimjanovszki I, Drotos G, et al. Is there any differences between the findings of Clock Drawing Tests if the clock shows different times? J Alzheimers Dis. 2014;39:749-57. Semi-quantitative systems also utilize a subjective approach, in which the whole clock is analyzed, but a numerical scale is used to characterize a quantitative domain. Two examples are the methods proposed by Sunderland et al.1010. Sunderland T, Hill JL, Mellow AM, Lawlor BA, Gundersheimer J, Newhouse PA, et al. Clock drawing in Alzheimer's disease: a novel measure of dementia severity. J Am Geriatr Soc . 1989;37:725-9. and Shulman et al..2626. Shulman KI, Gold DP, Cohen CA, Zucchero CA. Clock-drawing and dementia in the community: a longitudinal study. Int J Geriatr Psychiatry . 1993;8:487-96.,2424. Ehreke L, Luck T, Luppa M, König HH, Villringer A, Riedel-Heller SG. Clock drawing test: screening utility for mild cognitive impairment according to different scoring systems: results of the Leipzig Longitudinal Study of the Aged (LEILA 75+).Int Psychogeriatr . 2011;23:1592-601. Table 1 illustrates the different classifications of CDT scoring systems and the chronological changes they have undergone over the years.

Initially, the scoring systems used a semi-quantitative approach (Table 1). The CDT was then used as a medical screening tool to diagnose cognitive deficits in dementia and delirium. No interest was expressed in specific aspects of errors made during the CDT because it was simply used to differentiate healthy older adults from those with dementia.

The CDT meets the criteria for a cognitive screening instrument. It is quick to apply, well accepted by patients, easy to score, and relatively independent of language, education, and culture. It also has good inter-rater and test-retest reliability, high levels of sensitivity and specificity, concurrent validity, and predictive validity. Because of these attributes, it has seen widespread clinical use.1313. Shulman KI. Clock-drawing: is it the ideal cognitive screening test? Int J Geriatr Psychiatry . 2000;15:548-61.

Shulman1313. Shulman KI. Clock-drawing: is it the ideal cognitive screening test? Int J Geriatr Psychiatry . 2000;15:548-61. reported mean levels of sensitivity and specificity of 85% among all scales analyzed from 1983 to 1998. Even so, because of difficulties in replicating the results, conceptual disagreement is still seen in the literature. In Brazil, Lourenço et al.2020. Lourenço RA, Ribeiro-Filho ST, de Freitas Henriques Moreira I, Paradela EMP, Miranda AS. The Clock Drawing Test: performance among elderly with low educational level. Rev Bras Psiquiatr. 2008;30:309-15. and Aprahamian et al.2727. Aprahamian I, Martinelli JE, Neri AL, Yassuda MS. The Clock Drawing Test: a review of its accuracy in screening for dementia. Dement Neuropsychol. 2009;3:74-80. compared different scoring methods and found they were equivalent. Although previous studies demonstrated this, opinions regarding which method should be adopted for the test's interpretation are far from reaching a consensus. Authors highlight the methods proposed by Shulman et al.,2626. Shulman KI, Gold DP, Cohen CA, Zucchero CA. Clock-drawing and dementia in the community: a longitudinal study. Int J Geriatr Psychiatry . 1993;8:487-96. Sunderland et al.,1010. Sunderland T, Hill JL, Mellow AM, Lawlor BA, Gundersheimer J, Newhouse PA, et al. Clock drawing in Alzheimer's disease: a novel measure of dementia severity. J Am Geriatr Soc . 1989;37:725-9. and Mendez et al.11. Mendez MF, Ala T, Underwood KL. Development of scoring criteria for the clock drawing task in Alzheimer's disease. J Am Geriatr Soc. 1992;40:1095-9. as the most accurate ones.1313. Shulman KI. Clock-drawing: is it the ideal cognitive screening test? Int J Geriatr Psychiatry . 2000;15:548-61.,28

Table 1
Different quantitative, semi-quantitative, and qualitative CDT scoring systems throughout the years.

HISTORICAL TRAJECTORY MILESTONES

Shulman et al.2929. Shulman KI, Shedletsky R, Silver IL. The challenge of time: clock-drawing and cognitive function in the elderly. Int J Geriatr Psychiatry . 1986;1:135-40. proposed one of the first scoring systems which remains one of the most widely used scales in the literature to this day.77. Shulman, K.I., Herrmann N, Brodaty H, Chiu H, Lawlor B, Ritchie K, et al. IPA survey of brief cognitive screening instruments. Int Psychogeriatr. 2006;18:281-94. It consists of a hierarchical scale (i.e., a scale with severity ratings), in which the clock is analyzed as a whole. The system was reviewed in 1993.1313. Shulman KI. Clock-drawing: is it the ideal cognitive screening test? Int J Geriatr Psychiatry . 2000;15:548-61.

Three years later, two other authors published new methods: Sunderland et al.10 and Wolf-Klein et al..3030. Wolf-Klein GP, Silverstone FA, Levy AP, Brod MS. Screening for Alzheimer's disease by clock drawing. J Am Geriatr Soc . 1989;37:730-4. Sunderland's method is still widely employed. It is more detailed and has categories of typical errors.1616. Pinto E, Peters R. Literature review of the Clock Drawing Test as a tool for cognitive screening. Dement Geriatr Cogn Disord. 2009;27:201-13. Wolf-Klein et al.3030. Wolf-Klein GP, Silverstone FA, Levy AP, Brod MS. Screening for Alzheimer's disease by clock drawing. J Am Geriatr Soc . 1989;37:730-4. used visual clock patterns instead of a hierarchical scale.

An increasing use of screening tests was evident, especially with older adults. However, during a second period in history, the use of quantitative scoring systems became more frequent, and more objective scoring methods were sought. Using a quantitative approach, the CDT could be scored faster and easier so was more readily applied by busy clinicians. At this point in time, the quantitative scoring system was important for the early identification and monitoring of dementia because of the growing number of older adults and high prevalence of cognitive impairment among them.

The scoring system proposed by Mendez et al.11. Mendez MF, Ala T, Underwood KL. Development of scoring criteria for the clock drawing task in Alzheimer's disease. J Am Geriatr Soc. 1992;40:1095-9. was a quantitative scale, referred to as the Clock Drawing Interpretation Scale (CDIS).1616. Pinto E, Peters R. Literature review of the Clock Drawing Test as a tool for cognitive screening. Dement Geriatr Cogn Disord. 2009;27:201-13. Similar to Sunderland's system, Mendez's system was also based on the frequency of errors committed in the CDT.5353. Mainland BJ, Amodeo S, Shulman KI. Multiple clock drawing scoring systems: simpler is better. Int J Geriatr Psychiatry . 2014;29:127-36. However, it did not take the whole clock into account. Instead, the evaluation was performed separately, focusing on one aspect of the clock at a time.2424. Ehreke L, Luck T, Luppa M, König HH, Villringer A, Riedel-Heller SG. Clock drawing test: screening utility for mild cognitive impairment according to different scoring systems: results of the Leipzig Longitudinal Study of the Aged (LEILA 75+).Int Psychogeriatr . 2011;23:1592-601.

In the same year, Tuokko et al.3131. Tuokko H, Hadjistavropoulos T, Miller JA, Beattie BL. The Clock Test: a sensitive measure to differentiate normal elderly from those with Alzheimer disease. J Am Geriatr Soc . 1992;40:579-84. developed a quantitative scoring system that demanded more from the participant compared with other systems.1414. Aprahamian I. O Teste do Desenho do Relógio no rastreio diagnóstico da doença de Alzheimer em idosos no Brasil. Dissertação de Mestrado. Campinas: Faculdade de Ciências Médicas da Universidade Estadual de Campinas; 2008. It consisted of three stages: clock drawing, setting, and reading.1616. Pinto E, Peters R. Literature review of the Clock Drawing Test as a tool for cognitive screening. Dement Geriatr Cogn Disord. 2009;27:201-13.,5151. Wang P, Shi L, Zhao Q, Hong Z, Guo Q. Longitudinal changes in clock drawing test (CDT): performance before and after cognitive decline. PLoS One 2014;9:e97873. This way of evaluating the drawing allowed the analysis of different cognitive abilities and comparisons of performance in each stage. This was necessary because constructional skills tend to decline in normal aging while abstract conceptualization (i.e., executive function) is preserved. The diagnosis of dementia depends in part on abstract thinking and reasoning, which are also important for clock reading and setting. Therefore, the method scored performance efficiency in general and also specific types of errors.

Quantitative scoring systems for the CDT are especially useful in moderate and severe dementia.5252. Ricci M, Pigliautile M, D'Ambrosio V, Ercolani S, Bianchini C, Ruggiero C, et al. The clock drawing test as a screening tool in mild cognitive impairment and very mild dementia: a new brief method of scoring and normative data in the elderly. Neurol Sci. 2016;37:867-73. Powlishta et al.5454. Powlishta KK, Von Dras DD, Stanford A, Carr DB, Tsering C, Miller JP, et al. The clock drawing test is a poor screen for very mild dementia. Neurology. 2002;59:898-903. suggested that mild dementia, particularly AD, can also be differentiated from normal aging based on the CDT, but its sensitivity for detecting very mild dementia is poor. This aspect needs to be highlighted because it can cause sub- or even misdiagnoses.5454. Powlishta KK, Von Dras DD, Stanford A, Carr DB, Tsering C, Miller JP, et al. The clock drawing test is a poor screen for very mild dementia. Neurology. 2002;59:898-903. The CDT is also not very useful for identifying individuals with mild cognitive impairment (MCI) because it does not allow descriptions of the participants' error profiles.5555. Fabricio AT, Aprahamian I, Yassuda MS. Qualitative analysis of the Clock Drawing Test by educational level and cognitive profile. Arq Neuropsiquiatr . 2014;72:289-95. At this point, the medical approach was no longer sufficient for detecting the transition from normal to pathological aging. It was necessary to refine and improve the method using a neuropsychological approach that analyzes information processing and its qualitative aspects. Understanding the ways in which older adults draw the clock solely by considering the final score became insufficient for differentiating groups. It became important to evaluate the executive functions involved in the task and the execution of the drawing by analyzing errors.

Qualitative approaches became more useful by analyzing error types and thus helping describe different dementia profiles.1111. Rouleau I, Salmon DP, Butters N, Kennedy KC, McGuire K. Quantitative and qualitative analyses of clock drawings in Alzheimer's and Huntington's disease. Brain Cogn. 1992;18:70-87.,5656. Kitabayashi Y, Ueda H, Narumoto J, Nakamura K, Kita H, Fukui K. Qualitative analyses of clock drawings in Alzheimer's disease and vascular dementia. Psychiatry Clin Neurosci. 2001;55:485-91. As such, qualitative scoring systems are helpful for differential diagnoses.5656. Kitabayashi Y, Ueda H, Narumoto J, Nakamura K, Kita H, Fukui K. Qualitative analyses of clock drawings in Alzheimer's disease and vascular dementia. Psychiatry Clin Neurosci. 2001;55:485-91.

The first study that used a qualitative scoring method was by Rouleau et al..1111. Rouleau I, Salmon DP, Butters N, Kennedy KC, McGuire K. Quantitative and qualitative analyses of clock drawings in Alzheimer's and Huntington's disease. Brain Cogn. 1992;18:70-87. To better differentiate cognitive deficits into two progressive types of dementia (i.e., Huntington's disease and AD), the authors used both quantitative and qualitative methods. The method proposed by Rouleau et al. was similar to the one used by Mendez et al..1 It also analyzes specific aspects of the clock separately. The quantitative part has three independent subscales: clock face, numbers, and hands. The qualitative error analysis proposed by Rouleau had six categories: clock size, graphic difficulties, stimulus-bond response, conceptual deficit, spatial and/or planning deficit, and perseveration.1111. Rouleau I, Salmon DP, Butters N, Kennedy KC, McGuire K. Quantitative and qualitative analyses of clock drawings in Alzheimer's and Huntington's disease. Brain Cogn. 1992;18:70-87.,5353. Mainland BJ, Amodeo S, Shulman KI. Multiple clock drawing scoring systems: simpler is better. Int J Geriatr Psychiatry . 2014;29:127-36.

Executive function domains, such as abstract conceptualization, planning, and cognitive flexibility, began to be analyzed. Visuoconstructional skills can decline in normal aging, but abstract conceptualization may remain intact.3131. Tuokko H, Hadjistavropoulos T, Miller JA, Beattie BL. The Clock Test: a sensitive measure to differentiate normal elderly from those with Alzheimer disease. J Am Geriatr Soc . 1992;40:579-84. Although Tuokko et al.3131. Tuokko H, Hadjistavropoulos T, Miller JA, Beattie BL. The Clock Test: a sensitive measure to differentiate normal elderly from those with Alzheimer disease. J Am Geriatr Soc . 1992;40:579-84. also highlighted abstract conceptualization, their scoring method did not thoroughly describe the patients' profiles as Rouleau's1111. Rouleau I, Salmon DP, Butters N, Kennedy KC, McGuire K. Quantitative and qualitative analyses of clock drawings in Alzheimer's and Huntington's disease. Brain Cogn. 1992;18:70-87. qualitative scoring system did.

Parallel to the evolution of CDT scoring methods at this point in history, a controlled trial of the cholinesterase inhibitor tacrine in AD produced results that confirmed its safety and efficacy for AD treatment. It was the first medication approved by the United States Food and Drug Administration for the treatment of cognitive deficits in AD.5757. Farlow M, Gracon SI, Hershey LA, Lewis KW, Sadowsky CH, Dolan-Ureno J. A controlled trial of tacrine in Alzheimer's disease. the Tacrine Study Group. JAMA. 1992;268:2523-9. However, although the medication had beneficial effects on cognition, it did not slow progression of the disease. The need for an earlier diagnosis of dementia was clear, and targeting early stages of dementia became fundamental. Starting treatment as soon as possible increased the chances of slowing the progression of the disease.5858. Engelhardt E, Brucki SM, Cavalcanti JL, Forlenza OV, Laks J, Vale FA. Departamento de Neurologia Cognitiva e do Envelhecimento da Academia Brasileira de Neurologia. Tratamento da Doença de Alzheimer: recomendações e sugestões do Departamento Científico de Neurologia Cognitiva e do Envelhecimento da Academia Brasileira de Neurologia. Arq Neuropsiquiatr . 2005;63:1104-12.

For such early diagnoses, it was necessary to analyze specific error patterns in clock drawing, especially with regard to executive function. The qualitative scoring systems of the CDT are better able to identify early cognitive decline,5555. Fabricio AT, Aprahamian I, Yassuda MS. Qualitative analysis of the Clock Drawing Test by educational level and cognitive profile. Arq Neuropsiquiatr . 2014;72:289-95. and such qualitative methods became the most widely employed.

Until 1998, although the types of scoring systems were changing, the main focus of the CDT was still visuoconstructive ability (Table 2). Although the CDT was considered a sensitive measure of "abstract thinking" and "complex behavior," no distinction was made between constructional errors and executive function errors.3838. Royall DR, Cordes JA, Polk M. CLOX: an executive clock drawing task. J Neurol Neurosurg Psychiatry. 1998;64:588-94. However, in 1998, Royall et al.3838. Royall DR, Cordes JA, Polk M. CLOX: an executive clock drawing task. J Neurol Neurosurg Psychiatry. 1998;64:588-94. created a new way of scoring the CDT that significantly impacted the historical evolution of the CDT, called CLOX. It was a quantitative method designed to specifically evaluate executive function.1616. Pinto E, Peters R. Literature review of the Clock Drawing Test as a tool for cognitive screening. Dement Geriatr Cogn Disord. 2009;27:201-13.,5353. Mainland BJ, Amodeo S, Shulman KI. Multiple clock drawing scoring systems: simpler is better. Int J Geriatr Psychiatry . 2014;29:127-36.

Alzheimer's disease affects temporal cortical regions before it affects the frontal cortex. Isolated executive function errors do not indicate early AD. Many non-AD diseases, such as other "reversible" dementias, might be more expected to produce executive function impairment.3838. Royall DR, Cordes JA, Polk M. CLOX: an executive clock drawing task. J Neurol Neurosurg Psychiatry. 1998;64:588-94. A scoring system that differentiates executive function and constructional skills is very important for the diagnosis of the different subtypes of MCI and also early stages of dementia.

Qualitative types of scoring continued to emerge. In 2000, Shulman1313. Shulman KI. Clock-drawing: is it the ideal cognitive screening test? Int J Geriatr Psychiatry . 2000;15:548-61. suggested that using a simple scoring system that emphasizes the qualitative aspects of clock drawing, together with a quantitative system, could maximize the utility of the test.

In 2011, Parsey and Schmitter-Edgecombe4747. Parsey CM, Schmitter-Edgecombe M. Quantitative and qualitative analyses of the clock drawing test in mild cognitive impairment and Alzheimer disease: evaluation of a modified scoring system. J Geriatr Psychiatry Neurol . 2011;24:108-18. demonstrated the accuracy of the CDT in distinguishing MCI, AD, and normal aging. Their qualitative scoring system was based on Rouleau et al..1111. Rouleau I, Salmon DP, Butters N, Kennedy KC, McGuire K. Quantitative and qualitative analyses of clock drawings in Alzheimer's and Huntington's disease. Brain Cogn. 1992;18:70-87. Combined with evaluations of error types, it became even more sensitive for the detection of MCI. It also highlighted the importance of qualitative scoring systems in the early identification of cognitive decline.5555. Fabricio AT, Aprahamian I, Yassuda MS. Qualitative analysis of the Clock Drawing Test by educational level and cognitive profile. Arq Neuropsiquiatr . 2014;72:289-95.

Today, there is an increasing tendency to use qualitative methods together with either quantitative or semi-quantitative methods. The emergence of more qualitative scoring systems4747. Parsey CM, Schmitter-Edgecombe M. Quantitative and qualitative analyses of the clock drawing test in mild cognitive impairment and Alzheimer disease: evaluation of a modified scoring system. J Geriatr Psychiatry Neurol . 2011;24:108-18.,5656. Kitabayashi Y, Ueda H, Narumoto J, Nakamura K, Kita H, Fukui K. Qualitative analyses of clock drawings in Alzheimer's disease and vascular dementia. Psychiatry Clin Neurosci. 2001;55:485-91. is attributable to the fact that solely quantitative methods are unable to describe subjects' error profiles or specific cognitive changes the way that qualitative studies can.5555. Fabricio AT, Aprahamian I, Yassuda MS. Qualitative analysis of the Clock Drawing Test by educational level and cognitive profile. Arq Neuropsiquiatr . 2014;72:289-95.

Another recent trend is that some scoring methods are beginning to be computerized.4848. Kim H, Cho YS, Do EI. Computational clock drawing analysis for cognitive impairment screening. In: Gross MD (Ed.), Proceedings of the Fifth International Conference on Tangible, Embedded, and Embodied Interaction. New York: ACM. 2011;297-300.,5959. Zorluoglu G, Kamasak ME, Tavacioglu L, Ozanar PO. A mobile application for cognitive screening of dementia. Comput Methods Programs Biomed. 2015;118:252-62. Such computerized methods analyze the entire construction process and not only the final drawing. Computerized systems enable the assessment of qualitative features, but the resulting score only indicates the presence or absence of dementia. Because the main goal is to screen for dementia, there is no qualitative score, and it does not thoroughly specify the neuropsychological characteristics of the drawing.4848. Kim H, Cho YS, Do EI. Computational clock drawing analysis for cognitive impairment screening. In: Gross MD (Ed.), Proceedings of the Fifth International Conference on Tangible, Embedded, and Embodied Interaction. New York: ACM. 2011;297-300.

SPECIFICITIES AND APPLICABILITY OF DIFFERENT SCORING SYSTEMS

As presented in Table 3, different types of CDT scoring systems have advantages and disadvantages. The best method to be applied depends on the specific situation.

Table 2
Historical changes in CDT scoring systems.

Table 3
Advantages and disadvantages of different types of scoring systems.

Several studies,2828. Storey JE, Rowland JTJ, Basic D, Conforti DA. A comparison of five clock scoring methods using ROC (receiver operating characteristic) curve analysis. Int J Geriatr Psychiatry . 2001;16:394-9.,5454. Powlishta KK, Von Dras DD, Stanford A, Carr DB, Tsering C, Miller JP, et al. The clock drawing test is a poor screen for very mild dementia. Neurology. 2002;59:898-903.,6060. Richardson HE, Glass JN. A comparison of scoring protocols on the Clock Drawing Test in relation to ease of use, diagnostic group, and correlations with Mini-Mental State Examination. J Am Geriatr Soc . 2002; 50:169-173.

61. Schramm U, Berger G, Muller R, Kratzsch T, Peters J, Frol­ich L. Psychometric properties of Clock Drawing Test and MMSE or Short Performance Test (SKT) in dementia screen­ing in a memory clinic population. Int J Geriatr Psychiatry . 2002;17:254-60.

62. Scanlan JM, Brush M, Quijano C, Borson S. Comparing clock tests for dementia screening: naïve judgments vs formal systems - what is optimal? Int J Geriatr Psychiatry . 2002;17:14-21.
-6363. Connor DJ, Seward JD, Bauer JA, Golden KS, Salmon DP. Performance of three scoring systems across different ranges of dementia severity. Alzheimer Dis Assoc Disord. 2005;19:119-27. including Brazilian ones,2020. Lourenço RA, Ribeiro-Filho ST, de Freitas Henriques Moreira I, Paradela EMP, Miranda AS. The Clock Drawing Test: performance among elderly with low educational level. Rev Bras Psiquiatr. 2008;30:309-15.,2727. Aprahamian I, Martinelli JE, Neri AL, Yassuda MS. The Clock Drawing Test: a review of its accuracy in screening for dementia. Dement Neuropsychol. 2009;3:74-80. have compared different CDT scoring methods. These comparisons usually evaluated reliability, correlations, and the importance of the instrument compared with other tests in the diagnosis of dementia in older adults. These studies concluded that the CDT can be scored reliably using a variety of scales and can accurately discriminate healthy individuals from older adults with dementia.

Because of the need for more specific and early diagnoses of pathologies and impairments, research on the preclinical stages of dementia, especially in AD, is increasingly focusing on the early detection of cognitive decline. It becomes crucial to characterize the cognitive profile that better predicts the progression from preclinical to clinical stages of the different subtypes of MCI and AD. Charchat-Fichman et al.6464. Charchat-Fichman H, Fernandes CS, Oliveira RM, Caramelli P, Aguiar D, Novaes R. O predomínio de Comprometimento Cognitivo Leve Disexecutivo em Idosos atendidos no ambulatório de Geriatria de um hospital público terciário na cidade do Rio de Janeiro. Rev Neuropsicol LatinoAmericana 2013;5[2]:31-40. highlight the diagnostic heterogeneity among transitional stages to dementia and the importance of understanding this heterogeneity for an earlier and more precise diagnosis.

Studies suggest that minimal cognitive alterations can be detected even before the criteria for MCI are met, thus enabling better predictions of possible progression to AD. However, the neuropsychological tests and scoring systems employed currently are still unable to detect such early stages.6565. Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM, et al. Toward defining the preclinical stages of Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement. 2011;7:280-92. Amodeo et al.6666. Amodeo S, Mainland BJ, Herrmann N, Shulman KI. The times they are a-changin': clock drawing and prediction of dementia. J Geriatr Psychiatry Neurol . 2015;28:145-55. stated that the CDT is useful for the longitudinal assessment of cognitive impairment. These authors also contended that, together with other tests, the CDT can predict conversion to dementia.

Other authors have further suggested that the analysis of a multidimensional test, such as the CDT, based only on a single numerical score tends to impair both the sensitivity and specificity of the instrument.6767. Fischer J, Loring D. Construction. In: Lezak M, Howieson D, Loring D, (Eds). Neuropsychological Assessment, 4th ed. New York: Oxford University Press ; 2004: 531-568. Therefore, a single-score quantitative method may not be able to detect subtle differences between healthy individuals and subjects with mild forms of cognitive impairment.2424. Ehreke L, Luck T, Luppa M, König HH, Villringer A, Riedel-Heller SG. Clock drawing test: screening utility for mild cognitive impairment according to different scoring systems: results of the Leipzig Longitudinal Study of the Aged (LEILA 75+).Int Psychogeriatr . 2011;23:1592-601. This specific approach also compromises the ability of the test to discriminate between different error types, which is imperative for differentiating AD from other cognitive disorders. Thus, exclusively using quantitative scoring methods does not yield the desired results, increasing the need for more studies on qualitative methods.55. Hubbard EJ, Santini V, Blankevoort CG, Volkers KM, Barrup MS, Byerly L, et al. Clock drawing performance in cognitively normal elderly. Arch Clin Neuropsychol. 2008;23:295-327.

Some studies have demonstrated the advantages of qualitative scoring methods for the CDT. Parsey and Schmitter-Edgecombe4747. Parsey CM, Schmitter-Edgecombe M. Quantitative and qualitative analyses of the clock drawing test in mild cognitive impairment and Alzheimer disease: evaluation of a modified scoring system. J Geriatr Psychiatry Neurol . 2011;24:108-18. and Fabricio et al.5555. Fabricio AT, Aprahamian I, Yassuda MS. Qualitative analysis of the Clock Drawing Test by educational level and cognitive profile. Arq Neuropsiquiatr . 2014;72:289-95. differentiated diagnostic groups using a qualitative method that could not have been achieved with quantitative analysis. Mendez et al.6868. Barrows RJ, Barsuglia J, Paholpak P, Eknoyan D, Sabodash V, Lee GJ, Mendez MF. Executive abilities as reflected by clock hand placement: frontotemporal dementia versus early-onset Alzheimer disease. J Geriatr Psychiatry Neurol . 2015;28:239-48. also illustrated that the analysis of specific errors, rather than global performance in clock drawing, is helpful for differentiating early-onset AD, behavioral variant frontotemporal dementia, and other conditions. Qualitative features were also more helpful than quantitative features for localizing lesion sites and differentiating subcortical and cortical cases of stroke.6969. Suhr J, Grace J, Allen J, Nadler J, McKenna M. Quantitative and qualitative performance of stroke versus normal elderly on six clock drawing systems. Arch Clin Neuropshychol. 1998;13:495-502.

CONCLUSION

The historical literature search performed in the present study revealed a great number of CDT scoring systems. Throughout the years, these different systems have changed and improved in several ways,5353. Mainland BJ, Amodeo S, Shulman KI. Multiple clock drawing scoring systems: simpler is better. Int J Geriatr Psychiatry . 2014;29:127-36. but direct comparisons between methods are often difficult because no consensus has been reached concerning the different methods.

It is generally agreed that the CDT is useful for detecting moderate and severe stages of dementia. Its ability to characterize MCI or even mild dementia is still controversial. There are divergent opinions regarding the different scoring systems because some are too complex and time consuming while others are too simplistic to have sufficient sensitivity and specificity.5252. Ricci M, Pigliautile M, D'Ambrosio V, Ercolani S, Bianchini C, Ruggiero C, et al. The clock drawing test as a screening tool in mild cognitive impairment and very mild dementia: a new brief method of scoring and normative data in the elderly. Neurol Sci. 2016;37:867-73.

In Brazil, different types of CDT quantitative methods are used1919. Paula JJ, Miranda DM, Moraes EN, Malloy-Diniz LF. Mapping the clock works: what does the Clock Drawing Test assess in normal and pathological aging? Arq Neuropsiquiatr. 2013;71:763-8. and studies conducted considering the role of formal education in the test.7070. Aprahamian I, Martinelli JE, Cecato J, Yassuda MS. Screening for Alzheimer's disease among illiterate elderly: accuracy analysis for multiple instruments. J Alzheimers Dis . 2011;26:221-9.,7171. Aprahamian I, Martinelli JE, Neri AL, Yassuda MS. The accuracy of the Clock Drawing Test compared to that of standard screening tests for Alzheimer's disease: results from a study of Brazilian elderly with heterogeneous educational backgrounds. Int Psychogeriatr . 2010;22: 64-71. However, few studies have employed qualitative scoring methods.5555. Fabricio AT, Aprahamian I, Yassuda MS. Qualitative analysis of the Clock Drawing Test by educational level and cognitive profile. Arq Neuropsiquiatr . 2014;72:289-95. Given the dearth of studies and the importance of the CDT for aging research, more studies on qualitative analyses of the CDT should be performed.

Another important aspect that should be more frequently addressed is the role of executive function. In Brazil, the CDT is used in the assessment of executive functions.7171. Aprahamian I, Martinelli JE, Neri AL, Yassuda MS. The accuracy of the Clock Drawing Test compared to that of standard screening tests for Alzheimer's disease: results from a study of Brazilian elderly with heterogeneous educational backgrounds. Int Psychogeriatr . 2010;22: 64-71. Paula et al.1919. Paula JJ, Miranda DM, Moraes EN, Malloy-Diniz LF. Mapping the clock works: what does the Clock Drawing Test assess in normal and pathological aging? Arq Neuropsiquiatr. 2013;71:763-8. highlighted in their study the importance of executive functions in CDT performance. However, as shown in the present historical review, very few studies have focused on this particular topic. Scoring methods usually consider the types of errors and specific features of the drawing, but none of them evaluate the planning strategies used by subjects during execution of the drawing.

A wide range of studies have presented different CDT scoring systems, since 1986, when it was first used as a screening instrument. This large number precluded discussion of all methods in this study, where the limitation of the study was failure to describe all of them. Thus, the articles were selected based on their historical importance. On the other hand, the study suggests possible future studies on CDT scoring criteria with a focus on executive functions and also as a system for the specific evaluation of planning strategies.

In summary, historically rooted discussions of the CDT and a better path to improving its scoring methods are warranted. Different clinical needs and circumstances throughout history have molded this path and led to the present tendencies in scoring methods. Despite the advantages and disadvantages of each scoring method, the current tendency of employing both quantitative/semi-quantitative and qualitative approaches provides a better understanding of patients and more precise diagnoses. Qualitative aspects complement quantitative ones, making the CDT a complex tool for investigating cognition during the aging process. Although qualitative analyses require specific training, their inclusion into neuropsychological assessments is appropriate and much needed.

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  • Funding. This study was supported by a master's scholarship from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).
  • 3
    This study was conducted at the Department of Psychology, Pontifical Catholic University of Rio de Janeiro RJ - Brazil

Publication Dates

  • Publication in this collection
    Jan-Mar 2017

History

  • Received
    19 July 2016
  • Accepted
    26 Oct 2016
Academia Brasileira de Neurologia, Departamento de Neurologia Cognitiva e Envelhecimento R. Vergueiro, 1353 sl.1404 - Ed. Top Towers Offices, Torre Norte, São Paulo, SP, Brazil, CEP 04101-000, Tel.: +55 11 5084-9463 | +55 11 5083-3876 - São Paulo - SP - Brazil
E-mail: revistadementia@abneuro.org.br | demneuropsy@uol.com.br