Twenty Years After Spinnler and Tognoni: New Instruments in the Italian Neuropsychologist’S Toolbox

Neurol Sci (2008) 29:000–000 DOI 10.1007/s10072-008-0864-y

ORIGINAL ARTICLE

Twenty years after Spinnler and Tognoni: new instruments in the Italian neuropsychologist’s toolbox

Angelo Bianchi • Mirko Dai Prà

Received: 18 January 2008 / Accepted in revised form 17 April 2008 © Springer-Verlag 2008

Abstract The aim of this article is to review neuropsycho- Introduction logical normative studies which – after Spinnler and Tognoni’s monograph of 1987 – were done on healthy In 1987 Spinnler and Tognoni [1] edited a vast collection of Italian adult subjects, and which either wholly or partially neuropsychological norms set on 321 healthy subjects over used the Equivalent Scores (ES) methodology proposed by the age of 40, chosen from several Italian regions, in col- Capitani et al. The independent norms settled for the same laboration with numerous centres specialized in the study tests have been compared in order to point out their agree- of cognitive deterioration. The collection consisted of 27 ment, measured by Cohen’s Kappa, which in most cases tests dealing with a wide range of cognitive functions: ori- resulted either excellent or good (>0.7). Available tests have entation, memory, attention, intelligence, language, praxia, been classified and arranged to facilitate the most suitable spatial cognition and visual perception. After the model of choice for different clinical purposes. Moreover, a simple covariance that best represented the contribution of demo- software program has been set up which adjusts and trans- graphic variable (sex, age, schooling) had been singled out forms raw scores into ES. As well as saving time and avoid- for every test, the raw scores were first adjusted and then ing errors, this simple aid is likely to improve the quality transformed into new standardized scores (named and clarity of the communication of neuropsychological Equivalent Scores, ES) on an ordinal scale ranging from 0 results. to 4, according to Capitani et al. [2–5]. The main point of ES methodology is to fix, with non- Keywords Neuropsychology · Assessment · Test · parametric techniques, the outer tolerance limit of the left Normative studies queue of the adjusted scores, so that it is possible to assess, with a known risk of error (<5%), the cut-off splitting the bottom 5% of the population: this segment of distribution is called ES=0, and represents pathological performance. At the other end of the scale, the adjusted scores higher than the median are called ES=4, while the remaining ES are used to divide the left half of the distribution into three approximately equivalent intervals. In addition, the methodology lets us accurately compare the performances from the various tests, so as to obtain, within the subject, a cognitive profile of the impaired and preserved functions. Spinnler and Tognoni’s work rapidly became a landmark for most Italian neuropsychologists, as has ES methodology. Besides the differential diagnosis between normal and patho- ౧ A. Bianchi ( ) · M. Dai Prà logical cognitive deterioration, the instrument has been Department of Mental Health, Via G. Monaco 13, increasingly applied in other clinical, rehabilitative and I-52100 Arezzo, Italy forensic settings. The complexities of these new applications e-mail: [email protected] – as well as the increasing development of neuropsychology 2 Neurol Sci (2008) 29:131–137

Table 1 Normative studies carried out on Italian samples A Studies adopting ES methodology integrally (n. 34)

Study, Year Test or Battery Sample Size Age Range Reference

Barigazzi et al., 1987 Prose memory 127 20-85 6 Orsini et al., 1987 Digit Span, Corsi 1355 20-99 7 Allamanno et al., 1987 Tower of London 131 40-88 8 Basso et al., 1987 Raven’s Coloured Progressive Matrices (CPM) 279 21-80 9 Capitani et al., 1988 Gottschaldt’s Hidden Figures Test 190 25-86 10 Borrini et al., 1989 Autobiographical Memory 157 55-89 11 Capitani et al., 1991 Corsi supraspan 495 25-85 12 Della Sala et al., 1992 Digit Cancellation Test 352 20-99 13 Capitani et al., 1992 Serial Position Curve 321 40-90 14 Brazzelli et al., 1993 Rivermead Behavioral Memory Test (RBMT) 231 18-70 15 Capitani et al., 1994 Prose Memory 228 40-80 16 Della Sala et al., 1995 Poppelreuter-Ghent’s Overlapping Figures Test 237 20-86 17 Papagno et al., 1995 Metaphor and Idioms Comprehension 322 19-94 18 Pomati et al., 1996 Odd-Man-Out Test, Classification and Recall of Figures 100 22-79 19 Giovagnoli et al., 1996 Trail Making Test 287 15-79 20 Carlesimo et al., 1996 Mental Deterioration Battery (MDB) 340 20-89 21 Mauri et al., 1997 Learning of Semantically Related and Unrelated Words 249 20-89 22 Barbarotto et al., 1998 Stroop Test 209 18-81 23 Laiacona et al., 2000 Wisconsin Card Sorting Test (WCST), Weigl Sorting Test 205 15-85 24 Caffarra et al., 2002 Rey’s Complex Figure (RCF) 280 20-89 25 Nichelli et al., 2002 Weight and Time Estimation Task (STEP) 121 20-79 26 Caffarra et al., 2002 Stroop Test (Short Form) 248 20-89 27 Rizzo et al., 2002 Famous Face Naming Test 187 21-70 28 Carlesimo et al., 2002 Rey’s Complex Figure, Short Story Recall 227 20-90 29 Caffarra et al., 2003 Raven’s Progressive Matrices 1938 (PM 38) 248 20-89 30 Caffarra et al., 2004 Modified Card Sorting Test (MCST) 248 20-90 31 Bizzozero et al., 2004 Past Famous Events Memory 96 46-75 32 Bizzozero et al., 2005 Famous Face Recognition Test 98 46-75 33 Rosci et al., 2005 Interpretation of a complex picture 196 20-89 34 Appollonio et al., 2005 Frontal Assessment Battery (FAB) 364 20-95 35 Bizzozero et al., 2007 Proper name comprehension 98 46-75 36 Bizzozero et al., 2007 Naming celebrities 98 46-75 37 Papagno et al., 2007 Metaphor Comprehension, figures 201 20-89 38 Anselmetti et al., 2008 BACS 204 20-89 39 B Studies adopting ES methodology partially (n. 17)

Study, Year Test or Battery Sample Size Age Range Reference Measso et al., 1993 Raven’s Coloured Progressive Matrices (CPM) 894 20-79 40 Measso et al., 1993 Mini Mental State Examination (MMSE) 906 20-79 41 Brazzelli et al., 1994 Milan Overall Dementia Assessment (MODA) 217 20-97 42 Zappalà et al., 1995 Phonological Word Fluency, Benton Visual Retention Test 701 20-79 43 (BVRT), Associate Learning Test Ghidoni et al., 1995 Autobiographical Memory 99 15-80 44 Capitani et al., 1998 Phonological Word Fluency 503 18-81 45 Caterini et al., 1998 Object recognition and orientation 174 20-85 46 Della Sala et al., 1998 Physiognomic decision 183 20-79 47 Capitani et al., 2000 Milner Landmark Task 240 25-95 48 Bizzozero et al., 2000 Face apraxia 180 20-94 49 Mariani et al., 2002 General Knowledge of the World 175 20-60 50 Budriesi et al., 2002 Past Famous Events Memory 169 21-77 51 Barbarotto et al., 2000 Picture reality decision 140 18-75 52 Della Sala et al., 2003 Cognitive Estimation Task (CET) 175 18-87 53 Della Sala et al., 2004 Gait apraxia 182 20-92 54 Iavarone et al., 2004 Frontal Assessment Battery (FAB) 236 20-80 55 Nocentini et al., 2006 Symbol Digit Modalities Test 361 20-80 56 C Studies adopting other methodologies (n. 2)

Study, Year Test or Battery Sample Size Age Range Reference Mondini et al., 2003 Short Neuropsychological Exam (ENB) 420 16-70 57 Heaton et al., 2000 Wisconsin Card Sorting Test (WCST) 560 6-70 58 Neurol Sci (2008) 29:131–137 3 as a specialist discipline – have fostered the research of new group B it is applied to the raw scores above the mean. The neuropsychological diagnostic tools, which have found a difference between the two parameters has constantly kind of “common language” in ES methodology. turned out to be irrelevant. This article aims to: ES=1, 2, 3: these divide the remaining left half of the 1. review the normative studies which – after Spinnler and distribution into three parts almost equivalent to percentile Tognoni’s monograph – were conducted on healthy intervals 5-20 (ES=1), 21-35 (ES=2), 36-50 (ES=3). In the Italian adult subjects. Most of these studies also exam- studies belonging to group B, which do not report the exact ined subjects under 40, filling an evident gap, mainly in non-parametric calculation of the middle ESs, they only neurotraumatology; represent an acceptable approximation of the “true” ESs. 2. compare the available norms in order to establish their Since ES 1 usually includes the inner tolerance limit, it can ratio of agreement; be labelled borderline. 3. propose some simple classifying standards to facilitate Finally, there is a third group of normative studies the choice of the most appropriate instruments in differ- (Table 1, C) which used completely different statistical ent settings; techniques. Normally, these studies utilize larger samples 4. illustrate the features of a simple scoring software pro- of subjects, do not adjust raw scores by regression equa- gram which both adjusts and transforms the raw scores tions and maintain stratified norms for age and schooling. into ES, saving time, avoiding errors and improving the For our purposes, only the studies that allow some sort of quality and clarity of the communication of results. comparison with the previous groups have been taken into consideration. For a complete review, see [59]. Although a purely descriptive comparison of the differ- Materials and methods ent norms is important, it is not enough to support or dis- claim the reliability of the method. It is necessary to Normative studies published since 1987 were collected. As demonstrate that the performance of the same subject even- not all studies were indexed, the principal biomedical and tually provides the same ES, when transformed by differ- psychological libraries were also surveyed, and some ent, independent norms. For this purpose, a simulated sam- experts in neuropsychological assessment methodology ple of 100 subjects was set up, balanced for sex, and repre- were consulted. senting the different ages and degrees of schooling includ- A total of 53 studies were collected [6-58], presenting ed in the empirical samples. Considering these variables, the norms for single, groups or whole batteries of tests, every simulated subject was attributed a raw score corre- which cover a wide range of cognitive functions (Table 1). sponding respectively to 10, 25, 50, 75 and 90% of the Most of these studies applied ES methodology integrally obtainable range (Table 2). (Table 1, A). Other studies applied it partially (Table 1, After adjusting and transforming the simulated scores B), but they can easily be compared since they used the by independent norms, the agreement of the resulting ESs same statistical techniques to adjust and set the cut-off was measured by Cohen’s Kappa, weighted for the degree score. Unlike the previous studies, they did not explicitly of disagreement [60]. use ES to indicate the various regions of distribution. Consequently, the comparison is possible on the basis of the following rules: Results ES=0: this is the same for both A and B groups, and is applied to the adjusted scores below the left outer tolerance Descriptive comparisons limit (bottom 5% of the population, with a probability of 95%). This cut-off, which is clinically the most important, In some cases, the concurrent tests, though nominally iden- is independent from the distribution form. tical, are not comparable at all because of the different ES=4: in the studies belonging to group A, this is materials or scoring methods. In other cases, even though applied to the adjusted scores above the median, while in the tests are the same, the normative samples are not simi-

Table 2 Simulated sample Schooling Age 5 8 13 17 20 10%, 25%, 50%, 75%, 90% 10%, 25%, 50%, 75%, 90% 10%, 25%, 50%, 75%, 90% 10%, 25%, 50%, 75%, 90% 35 10%, 25%, 50%, 75%, 90% 10%, 25%, 50%, 75%, 90% 10%, 25%, 50%, 75%, 90% 10%, 25%, 50%, 75%, 90% 50 10%, 25%, 50%, 75%, 90% 10%, 25%, 50%, 75%, 90% 10%, 25%, 50%, 75%, 90% 10%, 25%, 50%, 75%, 90% 65 10%, 25%, 50%, 75%, 90% 10%, 25%, 50%, 75%, 90% 10%, 25%, 50%, 75%, 90% 10%, 25%, 50%, 75%, 90% 75 10%, 25%, 50%, 75%, 90% 10%, 25%, 50%, 75%, 90% 10%, 25%, 50%, 75%, 90% 10%, 25%, 50%, 75%, 90% n=100; M=50; F=50; Females underlined 4 Neurol Sci (2008) 29:131–137 lar enough to allow any reliable comparison. Finally, the only this simulated subgroup (n=60). This clearly limits the possible descriptive comparisons, even where partial, are power of statistical test (Table 4). reported in Table 3.

Discussion Simulated sample Descriptive comparisons The only tests that can be compared are those belonging to groups A and B in Table 1. As regards the tests originally The phonological word fluency (FAS) test shows the great- included in Spinnler and Tognoni’s norms, since they est discrepancies in the concurrent studies. The most plau- included only subjects over 40, we decided to compare sible explanation concerns the composition of the norma-

Table 3 Descriptive comparisons between independent norms

Test Cut-off Mean/Median Norms

Phonological Word Fluency (FAS) 10.7 26.9 Zappalà et al., 1995 17.3 31.4 Carlesimo et al., 1996 Raven’s Coloured Progressive Matrices 18 29.8 Basso et al., 1987 18.6 27.6 Measso et al., 1993 18.9 27.7 Carlesimo et al., 1996 Digit span 3.5 5.9 Orsini et al., 1987 - 5.6 Mondini et al., 2003 Trail Making test - A - 45.4 Mondini et al., 2003 94 47.3 Giovagnoli et al., 1996 Trail Making test - B - 113.8 Mondini et al., 2003 283 116.2 Giovagnoli et al., 1996 WCST – perseverative errors (age 60-69, schooling <13) - 25.8 Laiacona et al., 2000 - 26.0 Heaton et al., 2000 Frontal Assessment Battery (FAB) 11.5 15.3 Iavarone et al., 2004 13.5 16.1 Appollonio et al., 2005 Rey’s 15 Words - Immediate Recall 28.5 42.3 Carlesimo et al., 1996 25.1 39.3 Mauri et al., 1997 Rey’s 15 Words - Delayed Recall 4.6 8.9 Carlesimo et al., 1996 3.4 8.3 Mauri et al., 1997 Rey’s Complex Figure – Delayed Recall 6.3 16.9 Carlesimo et al., 2002 9.4 14.7 Caffarra et al., 2002 Progressive Matrices 1938 (age >40) - 34.3 Caffarra et al., 2003 14.7 28.8 Spinnler and Tognoni, 1987 Weigl Sorting Test (age >40) - 12.0 Laiacona et al., 2000 4.2 10.8 Spinnler and Tognoni, 1987

Table 4 ES agreement between independent norms in the simulated sample Compared norms Kw se 95% CIs

CPM: Basso - Measso 0.734 0.052 0.632–0.836 Basso - Carlesimo 0.731 0.053 0.627–0.835 Measso - Carlesimo 0.842 0.044 0.738–0.910 FAS: Carlesimo-Zappalà 0.703 0.052 0.601–0.805 Rey’s Complex Figure (Delayed): Caffarra-Carlesimo 0.783 0.049 0.687–0.879 Rey’s 15 words (Immediate): Carlesimo-Mauri 0.902 0.037 0.829–0.974 Rey’s 15 words (Delayed): Carlesimo-Mauri 0.699 0.052 0.597–0.801 PM 38 (age>40; n=60): Spinnler-Caffarra 0.622 0.069 0.487–0.757 Weigl (age>40; n=60): Spinnler-Laiacona 0.511 0.076 0.276–0.657 FAB: Appollonio-Iavarone 0.335 0.051 0.235–0.435 n=100 or 60 Neurol Sci (2008) 29:131–137 5 tive samples. Zappalà’s sample, the most numerous, is also Spinnler and Tognoni’s norms, only regarding the subjects the most representative of the less educated population: the over 40. The difference between the means is about 1.5 raw subjects with the lowest schooling (up to 3 years, virtually score for the Weigl (in a range from 0 to 15), and 4.5 raw illiterate) account for 13% of the total, a percentage which score for the PM 38 (in a range from 0 to 48), which is is bound to weigh heavily on the performance of the whole about 10% for both the more recent studies. group. Carlesimo’s sample, in contrast, intentionally excludes this section of the population. If we do not consid- er the contribution of this part of the sample, the general Simulated sample means of the two studies are very close (30.2 vs 31.4). In clinical use, it seems better to adopt Zappalà’s norms What counts much more than descriptive differences is that when the subject being examined has a very low sociocul- the same subject is classified in the same ES by independ- tural background: illiterate or minimally literate, subjects ent norms. In most comparisons the agreement ratio is good from particularly deprived zones or conditions, or first gen- or excellent, constantly over 0.7. eration immigrants. In these circumstances, the risk of a The two tests originally included in Spinnler and false positive classification is reduced. On the other hand, Tognoni’s norms, although showing a lower agreement the use of Carlesimo’s norms seems to be recommended ratio, do not seem to deviate from the general tendency, when subjects have at least an elementary level of school- taking into consideration the lower size of the sample. ing without any notable risk factors for cultural deprivation. The only test that shows a fair agreement ratio is the The other comparisons reveal more concordant results, FAB. The most plausible explanation concerns the nature in spite of some marginal differences. Of particular note is of the test itself, which makes it intrinsically less reliable. the almost perfect coincidence between the results of the Actually, FAB is not a true neuropsychological test, but a three different norms of the Coloured Progressive composite multidimensional battery, including both cogni- Matrices, confirming that it is an excellent example of a tive and psychomotor tasks. culture-fair test. The same goes for the Digit Span test, In clinical practice, it should be borne in mind that whose results have remained unchanged for over 15 years, Iavarone’s norm is less sensitive than Appollonio’s, in that without any cohort effect. it tends to classify a lower number of subjects (60 vs 75%) The concordance is also satisfying for the Trail as pathological (ES=0). On the other hand, a subject classi- Making Test, which shows an almost perfect concurrence fied as pathological by Iavarone’s norm will be more like- in part A, and only a minimal gap in part B, which is a far ly to actually be so (high specificity). more complex task and, therefore, more prone to contex- tual interference. The same can also be said for the Wisconsin Card Neuropyschological toolbox: instructions for use Sorting Test, one of the most complex both for the exami- nee and the examiner, from which one might have expect- In spite of the great quantity and high quality of tests, there ed a greater degree of variability: the results coincide are few clinical studies which have used them. Of the texts almost perfectly in this case too, although they are possible examined, many have never been used with any clinical only for the parameter concerning perseverative errors. population. The comparison between the two studies on Frontal On the other hand, the large amount of work done by Assessment Battery, performed almost at the same time on Italian neuropsychologists finds very little space in scientif- independent samples, shows only a minimal difference in ic literature, with dangerous effects on the social prestige, the medians, while the outer tolerance limit shows a more and perhaps also on the economic value of the discipline. remarkable difference, equal to about 2 raw scores (in a For these reasons we suggest some recommendations for range from 0 to 18). a more rational use of the available neuropsychological tools. The comparison between Rey’s 15 Words and an equivalent test (16 Semantically Unrelated Words) shows mar- Tests for dementia ginal differences in delayed recall, while immediate recall shows a modest discrepancy in favour of the former test One of the tasks that clinical neuropsychologists are more (about 3 raw scores in a range from 0 to 75 or 80). frequently asked to undertake is to confirm the diagnostic Rey’s Complex Figure shows the same discrepancy suspicion of dementia. A high percentage of referred sub- (about 3 raw scores) for the delayed recall score, but on a jects are in an advanced phase of illness. In these cases, range from 0 to 36 that amounts to a difference of nearly more than with diagnostic confirmation, neuropsychologi- 10%. The recall of Complex Figure is a very difficult task cal assessment has to do with defining the severity of the also for normal subjects, and so more apt to amplify possi- illness, also in view of social and legal interventions. In ble differences in the composition of normative samples. addition to diagnostic questions, neuropsychologists are The last two tests, the Weigl Sorting Test and Raven’s often entrusted with monitoring clinical conditions and Progressive Matrices 1938, allow a direct comparison with response to treatments. 6 Neurol Sci (2008) 29:131–137

For these kinds of issues, neuropsychologists can use Tests for cognitive deterioration in preclinical stage the following instruments: - Mini Mental State Examination (MMSE); Subjects who report memory complaints beginning from - Milan Overall Dementia Assessment (MODA); advanced adult age are candidates for a deep neuropsycho- - Frontal Assessment Battery (FAB); logical assessment aimed at early detection of preclinical - Rivermead Behavioral Memory Test (RBMT). cognitive impairment (Mild Cognitive Impairment, MCI). Unlike other batteries widely used for the early diagno- These subjects are usually within the normal range of the sis of dementia (e.g. Mental Deterioration Battery, MDB), instruments previously described, which are not sensitive these instruments provide only one overall cut-off. When enough to this kind of disorder. A high percentage of the administered to normal subjects, like in normative studies, subjects examined (the so called worried well) prove to be they tend to show results grouped near the upper limit of normal, while others show slight disorders which are not the scale. In other words, they are “easy” tests for most nor- confirmed or do not show any progression in subsequent mal subjects, and as such they have high specificity to exams. Yet, a significant percentage proceed to clinical detect possible cognitive disturbances, but not as high sen- forms of dementia. sitivity. Put simply, if a subject fails this kind of tests, it is The most appropriate instruments to detect MCI could almost certain that he/she will show worse results with be selected from among the following: more “difficult” tests. Other neuropsychological tests share this feature, and - Rey’s 15 words; can be used for the same purpose. A very effective criteri- - Learning of semantically related words; on for assessing the “easiness” of a test consists in compar- - Rey’s Complex Figure; ing the mean or median obtained by normal subjects with - Benton Visual Retention Test. the maximum score obtainable: the more they tend to coincide, the “easier” the test. These are all tests of anterograde episodic memory, ver- The cut-off of these tests leaves on the left such a wide bal and nonverbal respectively. range of scores to justify the attempt to single out at least The first, Rey’s 15 words, which is included in the three regions corresponding to as many levels of severity. Mental Deterioration Battery (MDB), has already proved This simple procedure, which is basically a refinement of particularly useful for the early diagnosis of MCI [64, 65]. the ES methodology, can greatly improve the informative Moreover, it also has parallel forms. value of neuropsychological assessment. The second test is derived from the California Verbal Regarding MMSE and MODA, two comparative stud- Learning Test and allows a not only quantitative but also ies [61, 62] acknowledge more sensitivity to MODA than qualitative evaluation of memory strategies used by exami- to MMSE, in the frame of a high correlation along the nees (semantic clustering). whole distribution of the scores. On this basis, a simple for- The other tests are also valid instruments for measuring mula has been proposed to convert the scores from one test not only nonverbal anterograde memory, but also spatial to the other, thus facilitating the comparison between stud- planning and constructional ability. ies which have used only one of the two. All these tests have ranges and cuts-offs which make FAB seems promising as a differential diagnostic possible the detection of even slight differences in perform- instrument between AD and FTD, since the latter would be ance, both between and within the subjects. more impaired than AD, clinical gravity being equal [55]. Other instruments can clearly be added to this core The neuropsychologist can add RBMT, which is one of assessment of episodic memory in its different compo- the best instruments for the ecological assessment of mem- nents. Obviously, the higher the number of tests, the ory. Even though it was not created for dementia, it is very stronger the probability of producing false positives. effective in assessing residual abilities in advanced phases of illness. Comprehensive neuropsychological assessment If it is necessary to further describe abilities in very advanced stages, the neuropsychologist can use the short Neuropsychologists are often requested to describe and version (score 0–100) of the Severe Impairment Battery measure overall cognitive functioning, a kind of wide-spec- (SIB), which has an Italian validation in severely demented trum neuropsychological profile. The candidates are usual- patients [63]. ly young people or adults suffering from neurological, psy- This is an example of a test which measures such ele- chiatric or general medical diseases which are thought to mentary abilities to be taken for granted as part of the nor- have negative effects on cognition. Neuropsychological mal adult behavioural repertory (species-wide expecta- assessment is also becoming part of the protocols preced- tions). To the same category belong most neuropsycholog- ing invasive treatments, mainly in neurosurgery, in studies ical tests used to assess the “classic” focal syndromes of behavioural genetics and in forensic settings. (aphasia, neglect, apraxia, agnosia), for which standardisa- A possible comprehensive neuropsychological battery tion on normal subjects is not required. is proposed in Table 5. Neurol Sci (2008) 29:131–137 7

Table 5 A short comprehensive neuropsychological battery

Cognitive Function Recommended Tests

Attention Digit Cancellation Test Trail Making A Short Term Memory Digit Span Corsi Verbal Episodic Memory Rey’s 15 words 16 Related and Unrelated Words Associate Learning Test Short Story Recall Non Verbal Episodic Memory Rey’s Complex Figure – Delayed Recall Executive Functions Phonological Word Fluency Trail Making B Wisconsin Card Sorting Test Reasoning Progressive Matrices 1938 Language Metaphor Comprehension Spatial Cognition Rey’s Complex Figure – Copy

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