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Key words Frontal assessment battery • FAB • Normative values • Test • Norms .... or major psychiatric diseases, a history of brain injury, stroke, dementia or any ...
Neurol Sci (2005) 26:108–116 DOI 10.1007/s10072-005-0443-4 ORIGINAL

I. Appollonio • M. Leone • V. Isella • F. Piamarta • T. Consoli • M.L. Villa • E. Forapani A. Russo • P. Nichelli

The Frontal Assessment Battery (FAB): normative values in an Italian population sample

Received: 19 December 2004 / Accepted in revised form: 11 May 2005

Abstract The Frontal Assessment Battery (FAB) is a short cognitive and behavioural six-subtest battery for the bedside screening of a global executive dysfunction; although recently devised, it is already extensively used thanks to its ease of administration and claimed sensitivity. The aim of the present study was to derive Italian normative values from a sample of 364 control subjects (215 women and 149 men) of different ages (mean: 57.4±17.9 years; range: 20–94 years) and educational level (mean: 10.4±4.3 years.; range: 1–17 years); the Mini Mental State Examination (MMSE) was concurrently administered. Multiple linear regression analysis revealed significant effects for age and education whereas gender was not significant; thus, from the derived linear equation, a correction grid for FAB raw scores was built. Based on nonparametric techniques, inferential cut-off scores were subsequently determined and equivalent scores (ES) computed. Test–restest and interrater reliabilities were both satisfactory. Interestingly, MMSE was significantly correlated with FAB raw scores, whereas adjusted scores were not. The present data may improve the accuracy in the use of the FAB both for clinical and research purposes. Key words Frontal assessment battery • FAB • Normative values • Test • Norms

I. Appollonio () • V. Isella • F. Piamarta • M.L. Villa E. Forapani • A. Russo Neurology Section, Department of Neurosciences University of Milano Bicocca, S. Gerardo Hospital Via Donizetti 106, I-20052 Monza (MI), Italy e-mail: [email protected] M. Leone • T. Consoli • P. Nichelli Neurological Department Policlinico Hospital University of Modena e Reggio Emilia Modena, Italy

Introduction The complexity of the executive system (with its behavioural, affective, motivational and cognitive components) is well known, and a number of experiments in animals, normal and brain-damaged subjects have recently documented both functional and anatomical dissociations among executive processes. The interpretation of dissociated deficits may differ according to conceptions of executive functions, but most theoretical approaches now suggest their anatomofunctional heterogeneity and propose the possibly to fragment the dysexecutive syndrome into several subsyndromes [1]. Moreover, although executive functions have traditionally been ascribed to the frontal lobes [2], impairment their has been also observed in patients with non-frontal lesions, i.e., after lesions involving deep structures such as the striatum or the thalamus. These studies have deeply influenced the approach, assessment and diagnosis of executive disorders. For clinical practice, they favour the search for a possible dysexecutive syndrome through the systematic assessment of its several components [3] (Table 1). Italian normative data on various executive tests are already available (see, for summary tables with corresponding references, MacPherson & Della Sala [4] and Capitani et al. [5]); the latest additions to these lists refer to the cognitive estimation task [6] and to abridged versions of the Stroop and Wisconsin Card tests [7, 8]. However, each of these tests usually relies on a single executive function, which is not necessarily impaired in cases of partial or mild frontal damage. Thus, the use of multiple tests appears mandatory for a comprehensive neuropsychological approach to a patient with clinical suspicion of a dysexecutive syndrome. Although such a “frontal battery” would allow, at least in principle, dissociation of the various cognitive components of an executive dysfunction, it would also be lengthy and cumbersome from a clinical perspective; in addition, none of the available normed executive tests takes into account extra-cognitive components.

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Table 1 Cognitive and behavioural disorders suggestive of a dysexecutive syndrome

Cognitive

Behavioural

Highly suggestive

Supportive features

- Response initiation; response suppression and focused attention - Rule deduction; maintenance and shifting of set - Problem-solving and planning - Information generation - Global hypoactivity (abulia, apathy, aspontaneity) - Global hyperactivity (distractibility, impulsivity disinhibition) - Perseveration and stereotyped behaviour - Environmental dependency (imitation and utilisation behaviour)

- Task coordination and divided attention; sustained attention - Strategic mnemonic processes

To overcome these problems, the Frontal Assessment Battery (FAB) was recently devised for the fast bedside screening of frontal functions [9]; six subtests were chosen based on lesional and functional literature data so that each of them was able to explore a specific cognitive or behavioural domain related to the frontal lobes: conceptualisation, mental flexibility, motor programming, sensitivity to interference, inhibitory control and environmental autonomy. The global performance on these six subtests gives a composite score summarising the severity of the dysexecutive syndrome, whereas individual subscores might suggest a descriptive pattern of executive dysfunction in a given patient. The same Authors performed a validation study [10] with patients suffering from different degenerative disorders known to involve the frontal lobes and showed that the FAB is a sensitive tool for these conditions. The aim of the present study was to collect normative data for the FAB in a large sample, to evaluate the effects of age, education and gender on performance and to calculate inferential cut-off scores. Moreover, a transformation of raw scores into equivalent scores (ES) was performed, following a technique that has been adopted for most neuropsychological tests carried out on the Italian population [11]. By removing differences in level of difficulty across tests, the ES achieved by a subject at the FAB can be easily comparable with the ES obtained by the same subject at other tests thus allowing a better characterisation of a patient’s cognitive profile [5, 12].

Subjects and methods Subjects The investigation was carried out on 364 subjects (215 women and 149 men) who varied widely in age and education (Table 2). They

- Theory of mind - Confabulation and reduplicative paramnesia - Anosognosia and anosodiaphoria - Disturbances of emotion and social behaviour - Disorders of sexual behaviour and control of micturition

were recruited in different districts of the provinces of Milan and Modena, both in rural or suburban areas and in city centres. Mean age for the whole sample was 57.4±17.9 years (range 20–94 years) and mean duration of education was 10.4±4.3 years (range 1–17 years, the latter being conventionally assigned to all subjects with a degree). All participants were community dwelling individuals who lived independently and were either working or otherwise engaged in activities in the community. Individuals were excluded if they had a current or past history of alcohol or drug abuse, current depression or major psychiatric diseases, a history of brain injury, stroke, dementia or any other neurological illness detected on a semistructured clinical interview. Subjects were also excluded if their adjusted score [13] at the Mini-Mental State Examination (MMSE) was lower than 24 out of 30. Only a negligible number of subjects were excluded based on this latter criterion. Subjects had also to be in good general health: endocrine disorders (particularly of the thyroid gland) or any systemic failure of clinical relevance were considered exclusion criteria; however, the inclusion criteria were not too selective, in order to avoid the sampling of a “hyper-normal” group; thus, individuals with mild hypertension or type II diabetes with a satisfactory drug treatment were not excluded. No instrumental or laboratory tests were carried out.

Procedures The original French and English versions of the FAB [9, 10] were each translated into Italian by one of the two Authors’ groups carrying out the present study, blinded to each other. The two translations were subsequently compared: minor inconsistencies were found and solved (the “prehension behaviour” subtest was positioned at the end of the battery; the sequence “fist-edgepalm” – instead of “edge-fist-palm” – was chosen in the motor series task after double checking with Luria’s original version); consistency was also reached on wording for all verbal instructions. Although instructions to each subtest could be repeated, they were usually immediately understood [14]1. The FAB test battery includes six subtests which were administered as follows:

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Table 2 Demographic distribution of the sample Education

Age (years)

(years)

20–29

1–3 4–5 6–8 9–13 >13 Total

– – 16 10 12 38

30–39

– – (M7/F9) 17 (M8/F9) (M4/F6) 13 (M7/F6) (M8/F4) 8 (M2/F6) (M19/F19) 38 (M17/F21)

40–49

50–59

60–69

70–79

80–89

– 5 (M5/F0) 12 (M3/F9) 7 (M2/F5) 6 (M5/F1) 30 (M15/F15)

1 (M0/F1) 11 (M5/F6) 12 (M2/F10) 27 (M10/F17) 15 (M6/F9) 66 (M23/F43)

2 (M0/F2) 26 (M6/F20) 18 (M8/F10) 32 (M14/F18) 19 (M15/F4) 97 (M43/F54)

2 (M0/F2) 16 (M6/F10) 17 (M4/F13) 25 (M9/F16) 7 (M6/F1) 67 (M25/F42)

2 5 6 1 5 19

(M0/F2) (M0/F5) (M1/F5) (M07F1) (M4/F1) (M5/F14)

90–95 – 4 (M1/F3) 3 (M1/F2) 1 (M0/F1) 1 (M0/F1) 9 (M2/F7)

Total 7 (M0/F7) 67 (M23/F44) 101 (M34/F67) 116 (M46/F70) 73 (M46/F27) 364 (M149/F215)

again after advising him/her not to take them. Sensory stimuli and environmental cues can activate patterns of responses that are normally inhibited; thus, this behavioural subtest assesses the spontaneous tendency to adhere to the environment and explores the domain of environmental independence. The score at each subtest may vary from 0 to 3 with a score of zero given when the subject fails to provide an answer or responds inappropriately. Thus, FAB total score may range from 0 to 18 and the administration of the entire battery requires approximately 10 min and little training. The subsequent analysis and scoring of subject’s performance takes 1–2 min.

(1) Similarities. Subjects have to identify the link between two objects from the same semantic category (i.e., an apple and a banana are both fruits); three pairs of objects are proposed. This cognitive subtest explores the domain of abstract reasoning/conceptualisation. (2) Phonological Verbal Fluency. Subjects are asked to produce in one minute as many words as they can beginning with the letter “S”. This cognitive subtest explores the domains of selforganised strategy and shifting i.e., mental flexibility. (3) Motor Series. Luria’s “fist-edge-palm” series has to be performed six times consecutively by the subject on his/her own, with the dominant hand. This behavioural subtest explores the domain of motor programming/planning. (4) Conflicting Instructions. Subjects must provide an opposite response to the examiner’s alternating signal, e.g. tapping once when the examiner taps twice and vice versa. Ten trials are run (5 trials with a single tapping and 5 trials with a double tapping); single and double tappings are intermixed in a fixed order. In this behavioural subtest, verbal commands conflict with sensory information and subjects should obey initial verbal command and refrain following what they see; thus, it explores the domain of sensitivity to interference. (5) Go-No Go Task. The same alternating signals used in the previous subtests are again given, but the subjects must now provide different responses, e.g., not tapping when the examiner taps twice and copying the examiner when he taps once. Ten intermixed trials are run, with the same sequence previously used. This behavioural subtest assesses the ability to withhold a response, inappropriately induced by both previous learning and concomitant sensory information, and explores the domain of inhibitory control. (6) Prehension Behaviour. Without saying anything or looking at the subject, the examiner touches both subject’s palms; if the subject spontaneously takes the hands, the examiner tries

Results Mean FAB raw score achieved by the whole sample was 16.1±1.8 (range: 9–18). Table 3 reports FAB descriptive statistics stratified by age and education: mean FAB scores are lower as age increases and as education decreases, indicating a worsening performance for older or less educated subjects. Table 4 shows the frequency distribution at each subtest: the two cognitive tests (“similarities” and “verbal fluency”) were those more fine-grained on the four levels of possible scoring; on the opposite, 357/364 subjects (98.1%) had a score of 3 and no one a score of 0 at the “prehension behaviour” task. Only a single score of 0 was given at each of the remaining three behavioural subtests, with only 2 additional subjects achieving a score of 1 at the “conflicting instructions” task. As a consequence, frequency distribution of the total FAB score was skewed towards higher values (Fig. 1).

Table 3 FAB mean scores (±SD) by age and education Education

Age (years)

(years)

20–29

30–39

40–49

50–59

60–69

70–79

80–89

90–95

Total

1–3 4–5 6–8 9–13 >13 Total

– – 15.9 (0.9) 16.9 (1.0) 17.9 (0.3) 16.8 (1.2)

– – 16.2 (1.3) 17.1 (1.0) 17.6 (0.5) 16.8 (1.2)

– 16.4 (0.9) 16.7 (1.2) 17.7 (0.5) 17.7 (0.5) 17.1 (1.0)

18.0 15.6 (1.4) 16.6 (0.8) 16.9 (1.1) 17.5 (0.9) 16.8 (1.2)

14.5 (0.7) 14.8 (1.3) 16.2 (1.3) 16.3 (1.2) 17.1 (0.8) 16.0 (1.4)

14.0 (2.8) 14.7 (2.0) 15.4 (2.2) 16.2 (1.8) 15.9 (1.0) 15.5 (2.0)

13.5 (2.1) 13.2 (1.3) 12.0 (1.3) 17.0 16.0 (2.3) 13.8 (2.3)

– 11.8 (2.1) 14.7 (1.5) 12.0 15.0 13.1 (2.1)

14.6 (2.1) 14.7 (1.8) 15.8 (1.7) 16.6 (1.4) 17.2 (1.2) 16.1 (1.8)

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Table 4 Frequency distributions of the scores at the single subtests of the FAB battery for the entire sample (n=364) Score

Subtest Similarities

Fluency

Luria’s Motor Series

Conflictual Instructions

Go–No Go Task

Prehension Behaviour

0

32 (8.8)

1 (0.3)

1 (0.3)

1 (0.3)

1 (0.3)

0 (0.0)

1

40 (11.0)

18 (4.9)

14 (3.8)

2 (0.5)

15 (4.1)

3 (0.8)

2

138 (37.9)

110 (30.2)

61 (16.8)

27 (7.4)

51 (14.0)

4 (1.1)

3

154 (42.3)

235 (64.6)

288 (79.1)

334 (91.8)

297 (81.6)

357 (98.1)

Numbers in brackets are percentages

30%

20%

10%

0% 9 10 11 FAB total score

12

13

14

15

16

17

Raw scores achieved by individuals on the FAB were entered into several linear regression analyses in order to check the relative influence of each demographic variables. The effects of age and education (years of schooling), were also studied after various transformations (logarithmic, quadratic, inverted, subtraction) and we adopted the transformation most effective in reducing the residual variance. Linear regression analysis was significant for gender (F(1,362)=9.4; p