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Are Cognitive Changes the First Symptoms of Huntington's Disease

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Are Cognitive Changes the First Symptoms of Huntington's Disease J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.64.2.172 on 1 February 1998. Downloaded from 172 J Neurol Neurosurg Psychiatry 1998;64:172–177 Are cognitive changes the first symptoms of Huntington’s disease? A study of gene carriers V Hahn-Barma, B Deweer, A Dürr, C Dodé, J Feingold, B Pillon, Y Agid, A Brice, B Dubois Abstract Huntington’s disease is an autosomal domi- Background—Huntington’s disease is a nant disorder with complete lifetime pen- neurodegenerative disorder due to an etrance, characterised by insidious onset of excessive number of CAG repeats in the symptoms associating choreic movements, af- IT15 gene on chromosome 4. The first fective disorders, and cognitive impairment.1 symptoms are typically choreic move- The diagnosis is typically based on the appear- ments or psychiatric disorders, whereas ance of the first motor symptoms, and global cognitive decline generally becomes confirmed by the presence of an excessive obvious later. This study was aimed at number (over 36) of CAG repeats in the IT15 2 detecting early subtle cognitive deficits in gene on chromosome 4. Together with genetic asymptomatic gene carriers. analysis, neuropsychological testing has been performed either on asymptomatic subjects at Methods—As part of the testing procedure for predictive diagnosis of Huntington’s high risk for Huntington’s disease (indirect method)3–5 or asymptomatic gene carriers disease, 91 asymptomatic at risk candi- 6–8 dates had a neuropsychological examin- (direct method). Some of these studies with neuropsychological evaluation have reported ation, evaluating global eYciency, that gene carriers were less eYcient than non- attention, memory (Wechsler memory carriers in the domains of executive functions scale and California verbal learning test), and, to a lesser degree, memory. However, the and executive functions. numbers of asymptomatic patients were rather Results—The groups of carriers (n=42) small in most studies and the diVerences were and non-carriers (n=49) diVered only on a neither robust nor consistently found.7 few memory variables. When we consid- One explanation for these inconsistent re- ered the group of gene carriers as a whole, sults may be that, in these studies, the groups of significant correlations emerged between gene carriers were considered as a whole, Fédération de the number of CAG repeats and (a) including variable proportions of both at risk Neurologie and performance on several tests of executive subjects with no cognitive impairment (pre- INSERM U.289, functions, and (b) performance on the sumably far from developing the disease) and Hôpital de la hard pairs associates of the Wechsler Salpêtrière, 47, at risk subjects with subtle cognitive impair- Boulevard de memory scale. Further analysis of per- ment. To avoid this confounding eVect, we l’Hôpital, 75013 Paris, formance on this memory subtest led to performed a three step analysis of the perform- http://jnnp.bmj.com/ France the division of the group of carriers into ance of gene carriers, (1) by comparing gene V Hahn-Barma two subgroups, without any overlap. The carriers and non-carriers on a large neuropsy- B Deweer performance of subjects without cognitive A Dürr chological battery, (2) by looking for correla- B Pillon deficits (n=32) was similar to that of non- tions between the number of CAG repeats and YAgid carriers on all tests. The subjects with eYciency on the neuropsychological tests A Brice cognitive deficits (n=10) diVered from within the group of gene carriers, and (3) by B Dubois both carriers without cognitive deficits subdividing the group of gene carriers into two and non-carriers over a wide array of subgroups on the basis of their performance on on September 26, 2021 by guest. Protected copyright. Laboratoire de Biochimie Génétique, variables measuring executive functions the memory subtest best correlated with CAG Hôpital Cochin, Paris and memory. Moreover, qualitative as- repeats. The underlying hypothesis was that France pects of the performance of carriers with gene carriers with cognitive impairment al- C Dodé cognitive deficits in the California verbal ready have Huntington’s disease, despite total learning test closely resembled those of lack of motor abnormalities, and will develop INSERM U 155, patients diagnosed as having Huntington’s the full range of the symptoms earlier than Château de Longchamp, Paris disease. normally eYcient gene carriers. If this hypoth- France Conclusion—This suggests that these sub- esis is valid, it should be possible to predict the J Feingold jects already have Huntington’s disease, onset of the disease in the absence of any motor despite a total lack of motor and psychiat- or aVective disorder, on the basis of some early Correspondence to: modifications of cognitive eYciency which Dr B Dubois, Fédération de ric signs. An ongoing follow up study is Neurologie and INSERM U testing the prediction that they will de- might constitute sensitive markers. 289, Hôpital de la velop the full range of symptoms of the Salpêtrière, 47 Boulevard de l’Hôpital, 75013 Paris, disease earlier than carriers without cog- France. Telephone 0033 1 42 nitive deficits. Methods and subjects 16 18 20 or 0033 1 42 16 22 INCLUSION PROCEDURE 02; fax 0033 1 44 24 36 58. During a period of three years, 99 candidates at (J Neurol Neurosurg Psychiatry 1998;64:172–177) the Salpêtrière Hospital, Paris, France, fol- Received 29 May 1997 and in revised form 31 July 1997 Keywords: Huntington’s disease; asymptomatic gene lowed the presymptomatic diagnosis procedure Accepted 22 August 1997 carriers; cognitive impairment until the genetic result. Of these, seven were J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.64.2.172 on 1 February 1998. Downloaded from Cognitive changes in asymptomatic Huntington’s disease gene carriers 173 excluded from this study on the basis of possi- NEUROPSYCHOLOGICAL TESTING bly confounding factors: concomitant neuro- The neuropsychological battery used included logical disorders (two), depression (two), various tests known to be sensitive to Hunting- advanced age >65 (two), education level <six ton’s disease,11–14 evaluating global cognitive years (one). Another subject was excluded after eYciency, attentional capacities, executive the genetic analysis because he was in the functions, and memory performance. Cogni- so-called intermediate zone (31 CAG repeats). tive eYciency was assessed with the mini men- Thus, 91 subjects (32 men and 59 women) tal state examination (MMSE)15 and the Mattis were included in the study; their mean age was dementia rating scale.16 Attentional capacities 33.3 (SD 8.1) (range 18–53) years; their mean were assessed by the digit span subtest of the level of education was 12.9 (SD 3.2) (range Wechsler adult intelligence scale revised,17 and 7–17) years. the Stroop test.18 In a previous study,19 we The standard procedure for predictive test- showed that in patients with choreic move- ing of Huntington’s disease was run by a ments, this battery correctly discriminates multidisciplinary team and included genetic between those with sporadic Huntington’s dis- counselling, neurological examination by a ease and those with non-Huntington’s disease neurologist specialised in Huntington’s dis- ease, psychological interviews, social evalua- chorea. tion, and neuropsychological testing. This Tests of executive functions included a score double blind clinical assessment lasted about of lexical fluency, corresponding to the sum of the words beginning with “P”, “R”, and “V” in three months before the molecular analysis was 20 undertaken. two minutes divided by three, the trail making 21 This procedure takes into account the test, with scores transformed into base 10 recommendations of the committee of the logarithms, and the digit symbol and arithme- International Huntington Association (IHA) tic subtests of the Wechsler adult intelligence and the World Federation of Neurology scale revised (WAIS-R). (WFN).9 All candidates included in the proce- Memory eYciency was evaluated with the dure for predictive diagnosis of Huntington’s Wechsler memory scale (WMS)22 with delayed disease were: (1) at risk—that is, with a family recall for logical memory, visual retention, and history of identified Huntington’s disease cases paired associates, and the California verbal (see below); (2) asymptomatic—that is, free of learning test (CVLT),23 which allows both any motor or psychiatric symptoms character- quantitative and qualitative assessment of istic of Huntington’s disease; (3) “consenting memory performance. This last test includes and informed”—that is, understanding and the following steps: (1) learning, in five trials, of accepting the test by written consent. a 16 item shopping list (Monday list) belonging to four embedded semantic categories; (2) CLINICAL ASSESSMENT acquisition in one trial of an interference list of An exhaustive interview carried out by the 16 shopping items (Tuesday list) belonging to geneticist and the neurologist verified the posi- four embedded semantic categories, of which tive family history of Huntington’s disease; the two are shared with the Monday list; (3) short clinical diagnosis of Huntington’s disease in delay free recall of the Monday list; (4) short aVected family members established the exist- delay cued recall of the Monday list, providing http://jnnp.bmj.com/ ence of an a priori risk in the candidate accord- the subject with each of the four category ing to the genealogy. All candidates were at a names to facilitate recall; (5) 20 minute delayed 50% risk, except one who was at 25%, because free recall of the Monday list; (6) delayed cued his at risk mother was still unaVected at 42 recall of the Monday list; (7) recognition of the years. Molecular confirmation for at least one Monday list items from various foils, including aVected relative was obtained in 90% (82 of interference list words that are semantically 91) of subjects. In the remainder, the clinical related or unrelated to target words; novel diagnosis in the aVected relatives was strongly words that are prototypical of the semantic cat- on September 26, 2021 by guest.
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