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Apathy in untreated, de novo patients with Parkinson’s disease: validation study of Apathy Evaluation Scale

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An Erratum to this article was published on 09 October 2014

Abstract

Apathy is a behavioural disturbance occurring alone or in concomitance with depression in Parkinson’s disease (PD). Here we present a validation study for the self-report version of the Apathy Evaluation Scale (AES-S), carried out in a sample of 60 non-demented, non-depressed untreated, drug-naïve, de novo PD patients; 20 patients of the sample (33.3 %) were classified as apathetic according to current clinical criteria. All enrolled patients completed the AES-S and a neurological and cognitive assessment. Mean AES-S score was 34.43. AES-S did not show floor or ceiling effect. Cronbach’s alpha was 0.872. Principal component analysis revealed three factors: the first (34.4 % of the variance) represented constitutive aspects of the construct of apathy; the second (8.5 % of the variance) represented a social dimension; the third factor (7.9 % of the variance) represented a dimension related to insight. With respect to clinical criteria for apathy considered as the gold standard, receiver operating characteristics curve analysis showed that a cut-off of 36/37 has the maximum discrimination power. High sensitivity and negative predictive values were obtained with cut-off scores of 33/34 or lower; high specificity and positive predictive values were obtained with cut-off scores of 38/39 or higher. AES-S score correlated with scores on frontal tasks, but not on Beck Depression Inventory, Unified Parkinson’s Disease Rating Scale, Hoehn and Yahr scale. The AES-S is a reliable and valid questionnaire for detecting apathy in PD. For screening purposes a 33/34 cut-off score is indicated, but a 38/39 cut-off score is necessary when a high specificity is desired.

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References

  1. Marin RS (1991) Apathy: a neuropsychiatric syndrome. J Neuropsychiatry Clin Neurosci 3:243–754

    Article  CAS  PubMed  Google Scholar 

  2. Pedersen KF, Larsen JP, Alves G, Aarsland D (2009) Prevalence and clinical correlates of apathy in Parkinson’s disease: a community-based study. Parkinsonism Relat Disord 15:295–299

    Article  PubMed  Google Scholar 

  3. Pluck GC, Brown RG (2002) Apathy in Parkinson’s disease. J Neurol Neurosurg Psychiatry 73:636–642

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Grossi D, Santangelo G, Barbarulo AM et al (2013) Apathy and related executive syndromes in dementia associated with Parkinson’s disease and in Alzheimer’s disease. Behav Neurol 27:515–522. doi:10.3233/BEN-129023

    Article  PubMed  Google Scholar 

  5. Lj Ziropadja, Stefanova E, Petrovic M, Stojkovic T, Kostic VS (2012) Apathy and depression in Parkinson’s disease: the Belgrade PD study report. Parkinsonism Relat Disord 18:339–342

    Article  Google Scholar 

  6. Cubo E, Benito-León J, Coronell C, Armesto D, ANIMO Study Group (2012) Clinical correlates of apathy in patients recently diagnosed with Parkinson’s disease: the ANIMO study. Neuroepidemiology 38:48–55

    Article  PubMed Central  PubMed  Google Scholar 

  7. Pedersen KF, Alves G, Brønnick K, Aarsland D, Tysnes OB, Larsen JP (2010) Apathy in drug-naïve patients with incident Parkinson’s disease: the Norwegian ParkWest study. J Neurol 257:217–223

    Article  PubMed  Google Scholar 

  8. Santangelo G, Vitale C, Trojano L et al (2012) Neuropsychological correlates of theory of mind in patients with early Parkinson’s disease. Mov Disord 27:98–105

    Article  PubMed  Google Scholar 

  9. Varanese S, Perfetti B, Ghilardi MF, Di Rocco A (2011) Apathy, but not depression, reflects inefficient cognitive strategies in Parkinson’s disease. PLoS ONE 6:e17846

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Dujardin K, Sockeel P, Delliaux M, Destée A, Defebvre L (2009) Apathy may herald cognitive decline and dementia in Parkinson’s disease. Mov Disord 24:2391–2397

    PubMed  Google Scholar 

  11. Martínez-Horta S, Pagonabarraga J, Fernández de Bobadilla R, García-Sanchez C, Kulisevsky J (2013) Apathy in Parkinson’s disease: more than just executive dysfunction. J Int Neuropsychol Soc 19:571–582

    Article  PubMed  Google Scholar 

  12. Santangelo G, Vitale C, Trojano L et al (2009) Relationship between depression and cognitive dysfunctions in Parkinson’s disease without dementia. J Neurol 256:632–638

    Article  CAS  PubMed  Google Scholar 

  13. Starkstein SE, Mayberg HS, Preziosi TJ, Andrezejewski P, Leiguarda R, Robinson RG (1992) Reliability, validity, and clinical correlates of apathy in Parkinson’s disease. J Neuropsychiatry Clin Neurosci 4:134–913

    Article  CAS  PubMed  Google Scholar 

  14. Zgaljardic DJ, Borod JC, Foldi NS et al (2007) Relationship between self-reported apathy and executive dysfunction in nondemented patients with Parkinson disease. Cogn Behav Neurol 20:184–192

    Article  PubMed Central  PubMed  Google Scholar 

  15. Butterfield LC, Cimino CR, Oelke LE, Hauser RA, Sanchez-Ramos J (2010) The independent influence of apathy and depression on cognitive functioning in Parkinson’s disease. Neuropsychology 24:721–730

    Article  PubMed  Google Scholar 

  16. Santangelo G, Morgante L, Savica R, Marconi R, Grasso L, Antonini A, De Gaspari D, Ottaviani D, Tiple D, Simoni L, Barone P, PRIAMO Study Group (2009) Anhedonia and cognitive impairment in Parkinson’s disease: Italian validation of the Snaith-Hamilton Pleasure Scale and its application in the clinical routine practice during the PRIAMO study. Parkinsonism Relat Disord 15:576–581

    Article  CAS  PubMed  Google Scholar 

  17. Benito-León J, Cubo E, Coronell C, ANIMO Study Group (2012) Impact of apathy on health-related quality of life in recently diagnosed Parkinson’s disease: the ANIMO study. Mov Disord 27:211–218

    Article  PubMed  Google Scholar 

  18. Santangelo G, Vitale C, Trojano L, Picillo M, Moccia M, Pisano G, Pezzella D, Cuoco S, Erro R, Longo K, Pellecchia MT, Amboni M, De Rosa A, De Michele G, Barone P (2014) Relationship between apathy and cognitive dysfunctions in de novo untreated Parkinson’s disease: a prospective longitudinal study. Eur J Neurol. doi:10.1111/ene.12467

    Google Scholar 

  19. Santangelo G, Trojano L, Barone P, Errico D, Grossi D, Vitale C (2013) Apathy in Parkinson’s disease: diagnosis, neuropsychological correlates, pathophysiology and treatment. Behav Neurol 27:501–513. doi:10.3233/BEN-129025

    Article  PubMed  Google Scholar 

  20. Leentjens AF, Dujardin K, Marsh L, Martinez-Martin P, Richard IH, Starkstein SE, Weintraub D, Sampaio C, Poewe W, Rascol O, Stebbins GT, Goetz CG (2008) Apathy and anhedonia rating scales in Parkinson’s disease: critique and recommendations. Mov Disord 23:2004–2014

    Article  PubMed  Google Scholar 

  21. Marin RS, Biedrzycki RC, Firinciogullari S (1991) Reliability and validity of the Apathy Evaluation Scale. Psychiatry Res 38:143–162

    Article  CAS  PubMed  Google Scholar 

  22. Kay DB, Kirsch-Darrow L, Zahodne LB, Okun MS, Bowers D (2012) Dimensions of apathy in Parkinson’s disease: exploratory factor analysis of the apathy scale. J Parkinsons Dis 2:161–166

    PubMed  Google Scholar 

  23. Pedersen KF, Alves G, Larsen JP, Tysnes OB, Møller SG, Brønnick K (2012) Psychometric properties of the Starkstein Apathy Scale in patients with early untreated Parkinson disease. Am J Geriatr Psychiatry 20:142–148

    Article  PubMed  Google Scholar 

  24. Robert PH, Onyike CU, Leentjens AFG, Dujardin K, Aalten P, Starkstein SE et al (2009) Proposed diagnostic criteria for apathy in Alzheimer’s disease and other neuropsychiatric disorders. Eur Psychiatry 24:98–104

    Article  CAS  PubMed  Google Scholar 

  25. Drijgers RL, Dujardin K, Reijnders JS, Defebvre L, Leentjens AF (2010) Validation of diagnostic criteria for apathy in Parkinson’s disease. Parkinsonism Relat Disord 16:656–660

    Article  PubMed  Google Scholar 

  26. Levy R, Dubois B (2006) Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cereb Cortex 16:916–928

    Article  PubMed  Google Scholar 

  27. McKinlay A, Grace RC, Dalrymple-Alford JC, Anderson TJ, Fink J, Roger D (2008) Neuropsychiatric problems in Parkinson’s disease: comparisons between self and caregiver report. Aging Ment Health 12:647–653

    Article  PubMed  Google Scholar 

  28. Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinicopathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders, 4th edn. DSM-IV-TR, American Psychiatric Association, Washington

    Google Scholar 

  30. Emre M, Aarsland D, Brown R et al (2007) Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 22:1689–1707

    Article  PubMed  Google Scholar 

  31. Santangelo G, Vitale C, Trojano L, De Gaspari D, Bilo L, Antonini A, Barone P (2010) Differential neuropsychological profiles in Parkinsonian patients with or without vascular lesions. Mov Disord 25:50–56

    Article  PubMed  Google Scholar 

  32. Folstein M, Folstein SE, McHugh PR (1975) Mini-Mental State: a practical method for grading the cognitive state of patients for the clinicians. J Psychiatr Res 12:189–198

    Article  CAS  PubMed  Google Scholar 

  33. Giovagnoli AR, Del Pesce M, Mascheroni S, Simoncelli M, Laiacona M, Capitani E (1996) Trail making test: normative values from 287 normal adult controls. Ital J Neurol Sci 17:305–309

    Article  CAS  PubMed  Google Scholar 

  34. Barbarotto R, Laiacona M, Frosio R et al (1998) A normative study on visual reaction times and two Stroop colour-word tests. Ital J Neurol Sci 19:161–170

    Article  CAS  PubMed  Google Scholar 

  35. Appollonio I, Leone M, Isella V, Piamarta F, Consoli T, Villa ML, Forapani E, Russo A, Nichelli P (2005) The frontal assessment battery (FAB): normative values in an Italian population sample. Neurol Sci 26:108–116

    Article  CAS  PubMed  Google Scholar 

  36. Visser M, Leentjens AF, Marinus J, Stiggelbout AM, van Hilten JJ (2006) Reliability and validity of the Beck depression inventory in patients with Parkinson’s disease. Mov Disord 21:668–672

    Article  PubMed  Google Scholar 

  37. Isella V, Appollonio I, Meregalli L, Melzi P, Iurlaro S, Frattola L (1998) Dati normativi per le versioni italiane delle scale di apatia e di anedonia. Archivio di psicologia, neurologia e psichiatria 59:356–375

    Google Scholar 

  38. Fahn S, Elton RL (1987) Members of the UPDRS Development Committee. In: Fahn S, Marsden CD, Calne D, Goldstein M (eds) Recent developments in Parkinson’s disease. MacMillan, Florham Park, pp 153–304

    Google Scholar 

  39. Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442

    Article  CAS  PubMed  Google Scholar 

  40. Hays RD, Anderson R, Revicki D (1993) Psychometric considerations in evaluating health-related quality of life measures. Qual Life Res 2:441–449

    Article  CAS  PubMed  Google Scholar 

  41. McHorney CA, Tarlov AR (1995) Individual-patient monitoring in clinical practice: are available health surveys adequate? Qual Life Res 4:293–307

    Article  CAS  PubMed  Google Scholar 

  42. Cronbach LJ (1951) Coefficient alpha and the internal structure of tests. Psychometrika 16:297–334

    Article  Google Scholar 

  43. Scientific Advisory Committee of the Medical Outcomes Trust (2002) Assessing health status and quality-of-life instruments: attributes and review criteria. Qual Life Res 11:193–205

    Article  Google Scholar 

  44. Nunnally JC, Bernstein IH (1994) Psychometric theory. McGraw- Hill, New York

    Google Scholar 

  45. Wyrwich KW, Nienaber MA, Tierney WM, Wolinsky FD (1999) Linking clinical relevance and statistical significance in evaluating intraindividual changes in health-related quality of life. Med Care 37:469–478

    Article  CAS  PubMed  Google Scholar 

  46. Guyatt GH, Berman LB, Townsend M, Pugsley SO, Chambers LW (1987) A measure of quality of life for clinical trials in chronic lung disease. Thorax 42:773–778

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Juniper EF, Guyatt GH, Jaeschke R (1996) How to develop and validate a new health-related quality of life instrument. In: Spilker B (ed) Quality of life and pharmacoeconomics in clinical trials, 2nd edn. Lippincott-Raven Publishers, Philadelphia, pp 49–56

    Google Scholar 

  48. Clarke DE, Rv Reekum, Simard M, Streiner DL, Freedman M, Conn D (2007) Apathy in dementia: an examination of the psychometric properties of the apathy evaluation scale. J Neuropsychiatry Clin Neurosci 19:57–64

    Article  PubMed  Google Scholar 

  49. Dujardin K, Sockeel P, Devos D, Delliaux M, Krystkowiak P, Destée A, Defebvre L (2007) Characteristics of apathy in Parkinson’s disease. Mov Disord 22:778–784

    Article  PubMed  Google Scholar 

  50. Stuss DT, Van Reekum R, Murphy KJ (2000) Differentiation of states and causes of apathy. In: Borod J (ed) The neuropsychology of emotion. Oxford University Press, New York, pp 340–363

    Google Scholar 

  51. Esposito F, Rochat L, Juillerat Van der Linden AC, Lekeu F, Charnallet A, Van der Linden M (2014) Apathy in aging: are lack of interest and lack of initiative dissociable? Arch Gerontol Geriatr 58:43–50

    Article  PubMed  Google Scholar 

  52. Stanton BR, Leigh PN, Howard RJ, Barker GJ, Brown RG (2013) Behavioural and emotional symptoms of apathy are associated with distinct patterns of brain atrophy in neurodegenerative disorders. J Neurol 260:2481–2490

    Article  PubMed  Google Scholar 

  53. Raimo S, Trojano L, Spitaleri D, Petretta V, Grossi D, Santangelo G. Apathy in Multiple Sclerosis: A validation study of the Apathy Evaluation Scale. J Neurol Sci

  54. Kirsch-Darrow L, Fernandez HH, Marsiske M, Okun MS, Bowers D (2006) Dissociating apathy and depression in Parkinson disease. Neurology 67:33–38

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  55. Isella V, Melzi P, Grimaldi M, Iurlaro S, Piolti R, Ferrarese C, Frattola L, Appollonio I (2002) Clinical, neuropsychological, and morphometric correlates of apathy in Parkinson’s disease. Mov Disord 17:366–371

    Article  PubMed  Google Scholar 

  56. Laatu S, Karrasch M, Martikainen K, Marttila R (2013) Apathy is associated with activities of daily living ability in Parkinson’s disease. Dement Geriatr Cogn Disord 35:249–255

    Article  CAS  PubMed  Google Scholar 

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Conflicts of interest

The authors declare that they have no conflict of interest.

Ethical standards

The present study has been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.

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Authors and Affiliations

  1. Department of Psychology, Second University of Naples, Caserta, Italy

    Gabriella Santangelo, Sofia Cuoco, Simona Raimo, Domenica Pezzella, Dario Grossi & Luigi Trojano

  2. IDC-Hermitage-Capodimonte, Naples, Italy

    Gabriella Santangelo, Marianna Amboni & Carmine Vitale

  3. Department of Medicine and Surgery, Neurodegenerative Diseases Center, University of Salerno, Salerno, Italy

    Paolo Barone, Sofia Cuoco, Marina Picillo & Maria Teresa Pellecchia

  4. Dipartimento di Scienze Neurologiche e del Movimento, Università di Verona, Verona, Italy

    Roberto Erro

  5. Sobell Department of Motor Neuroscience and Movement Disorders, University College London (UCL) Institute of Neurology, London, UK

    Roberto Erro

  6. Department of Neuroscience Reproductive and Odontostomatologic Sciences, University of Naples Federico II, Naples, Italy

    Marcello Moccia & Santangelo Franco

  7. University Parthenope, Naples, Italy

    Carmine Vitale

Authors
  1. Gabriella Santangelo
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  2. Paolo Barone
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  3. Sofia Cuoco
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  6. Marina Picillo
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Correspondence to Luigi Trojano.

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Santangelo, G., Barone, P., Cuoco, S. et al. Apathy in untreated, de novo patients with Parkinson’s disease: validation study of Apathy Evaluation Scale. J Neurol 261, 2319–2328 (2014). https://doi.org/10.1007/s00415-014-7498-1

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  • DOI: https://doi.org/10.1007/s00415-014-7498-1

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