Costa2014 Article StandardizationAndNormativeDat
Costa2014 Article StandardizationAndNormativeDat
DOI 10.1007/s10072-013-1520-8
ORIGINAL ARTICLE
Received: 18 April 2013 / Accepted: 7 August 2013 / Published online: 21 August 2013
Ó Springer-Verlag Italia 2013
Abstract The phonemic/semantic alternate fluency test to 90 years), a test consisting of the following three sub-
seems to overcome some limits of the instruments currently tests: (1) a single letter-cued (phonemic) fluency subtest;
used to assess set-shifting abilities. In particular, this test (2) a single category-cued (semantic) subtest; (3) a pho-
does not make high demands on motor systems because the nemic/semantic alternate fluency subtest. A composite
subject is required to rapidly change mental set to generate shifting index was also derived to capture the shifting cost
words by continuously alternating between phonemic and a subject pays passing from performance of the two single
semantic criteria. Thus, it is potentially feasible for use in fluency subtests to performance of the alternate fluency
individuals who have movement disorders. In this regard, subtest. We computed correction grids to adjust raw scores
some data support its sensitivity in revealing cognitive for age, literacy and gender according to the results of
impairments in people suffering from frontal–striatal-rela- regression analyses. Moreover, we computed equivalent
ted disorders. The first aim of this study was to provide scores to permit direct and fast comparison of performance
standardization and normative data for the phonemic/ on the three fluency tests.
semantic alternate fluency test. The second aim was to
upgrade normative data for the single phonemic and Keywords Set-shifting Fluency tests Cognitive
semantic fluency tests. For these purposes, we administered disorders Neuropsychological assessment
to a sample of 335 healthy Italian subjects (ranging from 20 Neurological diseases
M. Monaco C. Mundi
e-mail: [email protected] e-mail: [email protected]
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366 Neurol Sci (2014) 35:365–372
Number 29 29 67 67 57 39 47 335
Mean years of education [range 3–23] 15.17 13.9 12.58 11.31 11.49 10.44 10.06 11.88
and SD (1.77) (4.42) (4.16) (4.42) (5.03) (3.97) (4.58) (4.60)
M/F 12/17 13/16 28/39 20/47 27/30 21/18 25/22 146/189
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Neurol Sci (2014) 35:365–372 367
Fig. 1 The figure illustrates, in the whole sample, scores distribution of the fluency tests and of the composite shifting index as a function of
ageing (panels a and b) and of years of formal education (panels c and d)
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368 Neurol Sci (2014) 35:365–372
14.30
13.10
11.30
8.29
5.89
9.92
8.71
6.91
3.91
1.50
Table 2 Results of the multiple regression analysis for phonological
90
fluency task with gender and years of formal education as explicative
variables
7.30
4.89
8.92
7.72
5.92
2.91
0.51
13.31
12.11
10.30
Independent variables B Std. Err. df t p
85
Constant 18.27 1.52 2.332 11.98 0.000
Gender 3.17 1.01 2.332 3.15 0.001
9.31
6.30
3.90
7.93
6.73
4.92
1.92
-0.49
12.31
11.11
Education 1.11 0.11 2.332 10.23 0.000
80
8.32
5.31
2.91
6.93
5.73
3.93
0.92
-1.48
11.32
10.12
75
Table 3 Regression equation and correction grid according to gender
and education for raw scores on the phonological fluency
9.12
7.32
4.32
1.91
5.94
4.74
2.94
-0.07
-2.47
10.33
Education
70
3 5 8 13 17
9.33
8.13
6.33
3.32
0.92
4.95
3.74
1.94
-1.06
-3.47
Males 11.47 9.25 5.91 0.34 -4.12
Table 5 Regression equation and correction grid according to gender, age and education for raw scores on the semantic fluency
65
Females 8.30 6.07 2.73 -2.84 -7.29
Best linear model: 33.29–1.11*(School – 11.88) -1.59 for females;
8.34
7.14
5.33
2.33
-0.08
3.95
2.75
0.95
-2.06
-4.46
?1.59 for males
60
7.34
6.14
4.34
1.33
-1.07
2.96
1.76
-0.05
-3.05
-5.46
Table 4 Results of the multiple regression analysis for semantic
fluency task with gender, age and years of formal education as
55
1.96
0.76
-1.04
-4.05
-6.45
50
0.97
-0.23
-2.03
-5.04
-7.44
Age -0.20 0.03 3.331 -7.94 0.000
45
-0.02
-1.23
-3.03
-6.03
-8.44
40
-1.02
-2.22
-4.02
-7.03
-9.43
which also lasted 60 s each.
35
-2.01
-3.21
-5.02
-8.02
-10.43
-3.01
-4.21
-6.01
-9.02
-11.42
-4.00
-5.20
-7.01
0.39
13
17
3
5
8
3
5
8
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Neurol Sci (2014) 35:365–372 369
Table 6 Results of the multiple regression analysis for alternate determine which was the most effective in reducing
fluency task with gender and years of formal education as explicative residual variance. The effect of gender performance was
variables
determined using Student’s t test.
Independent variables B Std. Err. df t p We performed a multiple linear regression analysis for
each fluency sub-task and composite shifting index score,
Constant 27.81 2.56 3.331 10.88 0.000
with performance score as dependent variable and age,
Gender 3.50 0.98 3.331 3.57 0.000
education and gender as explicative factors. According to
Age -0.23 0.03 3.331 -7.99 0.000
Bonferroni’s correction, we inserted only variables with
Education 0.96 0.11 3.331 8.68 0.000
p B 0.017 (p = 0.05/3) in the final regression model.
Based on results of the multiple regression analyses,
aranciata) or to conjugate verbs. For each trial, the number regression equations were developed to calculate the
of legal words generated in 60 s was recorded. Perfor- adjusted performance scores for each combination of sig-
mance score in each subtest is the sum of the number of nificant demographic variables [27]. We used a non-para-
legal words generated in all trials belonging to that specific metric procedure to determine the lower (outer) and upper
subtest. A composite shifting index was computed that took (inner) limit of the tolerance interval for test performance
into account the words generated in all three subtests with confidence level of 95 % [35]. With 335 subjects, the
according to the following formula: total words generated outer limit, under which a performance may be considered
in the alternate fluency subtest/[(phonemic fluency abnormal, corresponds to the 11th scalar observation and
score ? semantic fluency score)/2]. This index is thought the inner limit, above which a performance may be con-
to capture the shifting cost a subject pays passing from sidered normal, to the 25th worst observation.
performing the single fluency subtests to performing the We classified adjusted scores into five categories (i.e.,
alternate fluency subtest. Equivalent Scores) [27] endowed with an ordinal rela-
tionship: 0 = scores lower than the 95 % tolerance limit;
Statistical analysis 4 = scores higher than the sample median; 1, 2 and
3 = scores lower than 10.4, 26.4 and 50 % of the norma-
A within-subjects ANOVA was executed to compare sub- tive sample distribution, respectively.
jects’ performance on the three fluency tests. Then, we
checked which demographic variables (age, education and
gender) affected healthy individuals’ raw performance Results
separately for each fluency task and the composite shifting
score. The relationship between explicative and dependents The effect of the within-subjects ANOVA was significant
variables was investigated by performing different regres- (F(2,668) = 345.5; p \ 0.001). A post hoc Tukey HSD
sion models (i.e. linear, cubic, quadratic and exponential) test showed that subjects’ performance on the phonemic/
and testing various transformations of the raw age and semantic fluency alternate test (mean = 28.4; SD = 11.3;
education values (i.e., quadratic, logarithmic, inverted) to range = 4–60; median = 28; mode = 30) was significantly
Table 7 Regression equation and correction grid according to gender, age and education for raw scores on the alternate fluency
Age/ 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90
education
Males
3 2.05 3.20 4.35 5.50 6.65 7.80 8.95 10.10 11.25 12.40 13.55 14.70 15.85 17.00 18.15
5 0.12 1.27 2.42 3.57 4.72 5.87 7.02 8.17 9.32 10.47 11.62 12.77 13.92 15.07 16.22
8 -2.77 -1.62 -0.47 0.68 1.83 2.98 4.13 5.28 6.43 7.58 8.73 9.88 11.03 12.18 13.33
13 -7.60 -6.45 -5.30 -4.15 -3.00 -1.85 -0.69 0.46 1.61 2.76 3.91 5.06 6.21 7.36 8.51
17 * -10.30 -9.15 -8.00 -6.85 -5.70 -4.55 -3.40 -2.25 -1.10 0.05 1.20 2.35 3.50 4.65
Females
3 -1.45 -0.30 0.85 2.00 3.15 4.30 5.45 6.60 7.75 8.90 10.05 11.20 12.35 13.50 14.65
5 -3.38 -2.23 -1.08 0.07 1.22 2.37 3.52 4.67 5.82 6.97 8.12 9.27 10.42 11.57 12.72
8 -6.28 -5.13 -3.98 -2.83 -1.68 -0.53 0.62 1.78 2.93 4.08 5.23 6.38 7.53 8.68 9.83
13 -11.10 -9.95 -8.80 -7.65 -6.50 -5.35 -4.20 -3.05 -1.90 -0.75 0.40 1.55 2.70 3.85 5.00
17 * -13.81 -12.66 -11.51 -10.36 -9.21 -8.06 -6.91 -5.76 -4.61 -3.46 -2.31 -1.15 0.00 1.15
Best linear model: 28.38-0.23*(Age-55.95)-0.96*(School-11.88) -1.75 for females; ?1.75 for males
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370 Neurol Sci (2014) 35:365–372
Table 8 Results of the multiple regression analysis for composite subjects’ score on all dependent variables (p \ 0.001 in all
shifting score with gender and years of formal education as explica- cases); gender predicted subjects’ ‘raw’ performance on all
tive variables
three fluency subtests (p \ 0.01), but not the composite
Independent variables B Std. Err. df t p shifting index values (p = 0.12); age predicted subjects’
performance on semantic and alternate fluency (p \ 0.001)
Constant 0.852 0.053 2.332 16.15 0.000
and composite shifting index scores (p \ 0.001), and ten-
Age -0.004 0.001 2.332 -5.91 0.000
ded to predict phonemic fluency test performance
Education 0.009 0.002 2.332 3.64 0.000
(p = 0.026). Using the regression equation values, we built
correction grids (Tables 2, 3, 4, 5, 6, 7, 8, 9). Cut-off
scores, with outer and inner tolerance limits, and equivalent
lower than that on both phonemic (mean = 33.3; scores are reported in Table 10.
SD = 10.5; range = 6–64; median = 34; mode = 35;
p \ 0.001) and semantic (mean = 41.3; SD = 9.5;
range = 6–70; median = 41; mode = 41; p \ 0.001) flu- Discussion
ency tests. In turn, subjects’ performance on the phonemic
fluency was significantly poorer than on the semantic flu- The main aim of this study was to obtain normative data on
ency subtest (p \ 0.001).1 a new test for the assessment of extradimensional shifting,
In the whole sample, the average value of the composite that is, the alternate fluency test [25]. This test consists of
shifting index was 0.75 (SD = 0.2; range 0.27–1.42); the following subtests: phonemic fluency, semantic fluency
median and mode were 0.76 and 0.8, respectively. and phonemic/semantic alternate fluency. No subject had
Age, years of formal education and gender were signif- difficulty in performing this 15-min test. As expected, it
icantly associated with all the fluency subtests and the was much more difficult to perform the alternate fluency
composite shifting index scores (Fig. 1). Females per- subtest than the two single fluency subtests. Age was
formed better than males in phonemic (mean = 34.42; inversely correlated with subjects’ alternate fluency per-
SD = 10.58 and mean = 31.82; SD = 10.3, respectively; formance and composite shifting index. Instead, higher
F(1,333) = 5.12; p = 0.024; Cohen’s d = 0.25), semantic educational level predicted better scores on both of the
(mean = 43.31; SD = 9.69 and mean = 38.64; SD = above-mentioned dependent measures. Gender also sig-
8.56, respectively; F(1,333) = 21.2; p \ 0.001; Cohen’s nificantly predicted performance on this subtest. Women
d = 0.51) and alternate (mean = 29.9; SD = 12.1 and were significantly more accurate than men. However, the
mean = 26.3; SD = 9.8, respectively; F(1,333) = 8.99; gender factor did not enter the regression equation for the
p \ 0.01; Cohen’s d = 0.33) fluency. As for the composite composite shifting index. Therefore, to adjust raw scores
shifting index, instead, no significant difference between and compute inferential cut-off scores for the alternate
females and males was found (mean = 0.76; SD = 0.22 phonemic/semantic fluency subtest, we considered results
and mean = 0.74; SD = 0.21, respectively; F(1,333) = of the regression equation including all three demographic
0.48; p [ 0.40; Cohen’s d = 0.15). As for age and years of factors, whereas for the composite shifting index only the
formal educations, the linear regression model was highly effect of years of formal education and age were consid-
effective in capturing the relationship with the dependent ered. Data were elaborated to calculate equivalent scores
variables (p \ 0.001 in all cases). Regarding age, in the [27] that allow direct comparisons between the three flu-
whole sample, a significant negative correlation was found ency tests.
with performance on phonemic fluency (r = -0.26; The phonemic/semantic alternate fluency test proposed
p \ 0.001), semantic fluency (r = -0.48; p \ 0.001), here is thought to tap shifting aptitude. In this test, the
alternate fluency (r = -0.49; p \ 0.001) and the composite subject is required to select words with the same phonemic
shifting index values (r = -0.37; p \ 0.001). Significant and semantic cues presented in the two single fluency
positive correlations were found among years of formal subtests administered previously. This should reduce the
education and scores on phonemic fluency (r = 0.46; effort needed to access the single letter or category-cued
p \ 0.001), semantic fluency (r = 0.36; p \ 0.001), alter- response. The key difference, with respect to the single
nate fluency (r = 0.45; p \ 0.001) and the composite fluency subtests, is the request to rapidly change mental set
shifting index values (r = 0.29; p \ 0.001). to generate words by continuously alternating between a
Results of multiple linear regression analyses showed phonemic and a semantic criterion. Therefore, the alternate
the following: years of formal education predicted fluency task could be effective for investigating the ability
to change mental set. However, it should be noted here that
1
Software used to calculate tolerance limits is freely available at the the fixed order of the administration of the three fluency
following online address: http://www1.fpl.fs.fed.us/nonpar.html. subtests could have somehow impacted the shifting cost
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Neurol Sci (2014) 35:365–372 371
Table 9 Regression equation and correction grid according to age and education for raw scores on the composite shifting score
A/E 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90
3 -0.05 -0.04 -0.02 0.00 0.02 0.04 0.06 0.07 0.09 0.11 0.13 0.15 0.17 0.19 0.20
5 -0.07 -0.05 -0.04 -0.02 0.00 0.02 0.04 0.06 0.08 0.09 0.11 0.13 0.15 0.17 0.19
8 -0.10 -0.08 -0.06 -0.04 -0.02 -0.01 0.01 0.03 0.05 0.07 0.09 0.10 0.12 0.14 0.16
13 -0.14 -0.12 -0.11 -0.09 -0.07 -0.05 -0.03 -0.01 0.01 0.02 0.04 0.06 0.08 0.10 0.12
17 * -0.16 -0.14 -0.12 -0.10 -0.09 -0.07 -0.05 -0.03 -0.01 0.01 0.03 0.04 0.06 0.08
Best linear model: 0.75-0.004*(Age-55.95)-0.009*(School-11.88)
Table 10 In the table we report cut-off and equivalent scores computed according to procedure described by Spinnler and Tognoni [30]
Outer limits Inner limits Equivalent scores
0 1 2 3 4
paid by subjects passing from executing the two single score similar to that previously reported by Carlesimo et al.
fluency subtests to performing the alternate fluency one. [33]; accuracy of the two samples does not, however,
This could be the reason why in the younger group we completely overlap. Indeed, on average, subjects in the
observe substantially the same performance on the pho- current study appeared to generate more words
nemic and alternate fluency subtests. This observation (mean = 33.3; SD = 10.5) than those in the sample studied
suggests caution in interpreting data from this age group. by Carlesimo et al. [33] (mean = 31.4; SD = 10.9).
As previously discussed, the test here proposed could Moreover, differently from what these authors observed
overcome some of the limits of tests currently used in Italy. [33], but in agreement with other investigations [7], we
Indeed, some of the instruments, such as the TMT, involve found that gender significantly affected performance (i.e.,
motor skills to a large extent. This could potentially reduce females were significantly more accurate than males); thus,
their usefulness in testing individuals with movement dis- this factor was taken into account to correct raw scores. As
orders. Other tests, such as the WCST or the WST, do not for the semantic fluency test, significant differences
allow for a pure measurement of shifting aptitude because emerged with respect to previously published data [27, 34].
they require the implementation of various other cognitive First, we found that gender significantly predicted accuracy,
processes (e.g., working memory, abstract reasoning). with females obtaining higher scores than males. Second,
Some studies have reported encouraging results using the we derived a cut-off score of 28.34, under which a perfor-
alternate fluency paradigm with patients suffering from mance could be defined as not normal. In a previous study in
frontal–striatal-related diseases [23–25]. Zec et al. [24] which a similar procedure was administered, a lower cut-off
demonstrated that, with respect to healthy controls, patients score (i.e., 24) was reported [34]. It could be argued that
with Parkinson’s disease were significantly more impaired above discrepancies, particularly those related to accuracy
on an alternate fluency than on a single phonemic fluency levels, were due to changes in some of the characteristics of
task. Pagonabarraga et al. [25] clearly documented that the the reference population (e.g., level of formal education),
performance of patients with Parkinson’s disease on an which may have significantly affected subjects’ perfor-
alternate verbal fluency test (similar to the one used in this mance. This indicates the importance of having up-to-date
study) independently discriminated between individuals standardization of the neuropsychological instruments.
with mild cognitive impairment and patients without any
cognitive deficits. In fact, the authors proposed including
this test in a cognitive scale to detect cognitive impair- References
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