Journal of Neurology

, Volume 261, Issue 12, pp 2319–2328 | Cite as

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

  • Gabriella Santangelo
  • Paolo Barone
  • Sofia Cuoco
  • Simona Raimo
  • Domenica Pezzella
  • Marina Picillo
  • Roberto Erro
  • Marcello Moccia
  • Maria Teresa Pellecchia
  • Marianna Amboni
  • Santangelo Franco
  • Dario Grossi
  • Luigi TrojanoEmail author
  • Carmine Vitale
Original Communication


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.


Parkinson’s disease Nonmotor symptoms Apathy Apathy Evaluation Scale Validation study Frontal executive dysfunctions 


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.

Supplementary material

415_2014_7498_MOESM1_ESM.docx (105 kb)
Supplementary material 1 (DOCX 105 kb)
415_2014_7498_MOESM2_ESM.docx (101 kb)
Supplementary material 2 (DOCX 100 kb)


  1. 1.
    Marin RS (1991) Apathy: a neuropsychiatric syndrome. J Neuropsychiatry Clin Neurosci 3:243–754CrossRefPubMedGoogle Scholar
  2. 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 15:295–299CrossRefPubMedGoogle Scholar
  3. 3.
    Pluck GC, Brown RG (2002) Apathy in Parkinson’s disease. J Neurol Neurosurg Psychiatry 73:636–642PubMedCentralCrossRefPubMedGoogle Scholar
  4. 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 CrossRefPubMedGoogle Scholar
  5. 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 18:339–342CrossRefGoogle Scholar
  6. 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 38:48–55PubMedCentralCrossRefPubMedGoogle Scholar
  7. 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 257:217–223CrossRefPubMedGoogle Scholar
  8. 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 27:98–105CrossRefPubMedGoogle Scholar
  9. 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:e17846PubMedCentralCrossRefPubMedGoogle Scholar
  10. 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 24:2391–2397PubMedGoogle Scholar
  11. 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 19:571–582CrossRefPubMedGoogle Scholar
  12. 12.
    Santangelo G, Vitale C, Trojano L et al (2009) Relationship between depression and cognitive dysfunctions in Parkinson’s disease without dementia. J Neurol 256:632–638CrossRefPubMedGoogle Scholar
  13. 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 4:134–913CrossRefPubMedGoogle Scholar
  14. 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 20:184–192PubMedCentralCrossRefPubMedGoogle Scholar
  15. 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 24:721–730CrossRefPubMedGoogle Scholar
  16. 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 15:576–581CrossRefPubMedGoogle Scholar
  17. 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 27:211–218CrossRefPubMedGoogle Scholar
  18. 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. 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 CrossRefPubMedGoogle Scholar
  20. 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 23:2004–2014CrossRefPubMedGoogle Scholar
  21. 21.
    Marin RS, Biedrzycki RC, Firinciogullari S (1991) Reliability and validity of the Apathy Evaluation Scale. Psychiatry Res 38:143–162CrossRefPubMedGoogle Scholar
  22. 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 2:161–166PubMedGoogle Scholar
  23. 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 20:142–148CrossRefPubMedGoogle Scholar
  24. 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 24:98–104CrossRefPubMedGoogle Scholar
  25. 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 16:656–660CrossRefPubMedGoogle Scholar
  26. 26.
    Levy R, Dubois B (2006) Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cereb Cortex 16:916–928CrossRefPubMedGoogle Scholar
  27. 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 12:647–653CrossRefPubMedGoogle Scholar
  28. 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 55:181–184PubMedCentralCrossRefPubMedGoogle Scholar
  29. 29.
    American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders, 4th edn. DSM-IV-TR, American Psychiatric Association, WashingtonGoogle Scholar
  30. 30.
    Emre M, Aarsland D, Brown R et al (2007) Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 22:1689–1707CrossRefPubMedGoogle Scholar
  31. 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 25:50–56CrossRefPubMedGoogle Scholar
  32. 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 12:189–198CrossRefPubMedGoogle Scholar
  33. 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 17:305–309CrossRefPubMedGoogle Scholar
  34. 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 19:161–170CrossRefPubMedGoogle Scholar
  35. 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 26:108–116CrossRefPubMedGoogle Scholar
  36. 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 21:668–672CrossRefPubMedGoogle Scholar
  37. 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 59:356–375Google Scholar
  38. 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 153–304Google Scholar
  39. 39.
    Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442CrossRefPubMedGoogle Scholar
  40. 40.
    Hays RD, Anderson R, Revicki D (1993) Psychometric considerations in evaluating health-related quality of life measures. Qual Life Res 2:441–449CrossRefPubMedGoogle Scholar
  41. 41.
    McHorney CA, Tarlov AR (1995) Individual-patient monitoring in clinical practice: are available health surveys adequate? Qual Life Res 4:293–307CrossRefPubMedGoogle Scholar
  42. 42.
    Cronbach LJ (1951) Coefficient alpha and the internal structure of tests. Psychometrika 16:297–334CrossRefGoogle Scholar
  43. 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 11:193–205CrossRefGoogle Scholar
  44. 44.
    Nunnally JC, Bernstein IH (1994) Psychometric theory. McGraw- Hill, New YorkGoogle Scholar
  45. 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 37:469–478CrossRefPubMedGoogle Scholar
  46. 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 42:773–778PubMedCentralCrossRefPubMedGoogle Scholar
  47. 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 49–56Google Scholar
  48. 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 19:57–64CrossRefPubMedGoogle Scholar
  49. 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 22:778–784CrossRefPubMedGoogle Scholar
  50. 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 340–363Google Scholar
  51. 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 58:43–50CrossRefPubMedGoogle Scholar
  52. 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 260:2481–2490CrossRefPubMedGoogle Scholar
  53. 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 SciGoogle Scholar
  54. 54.
    Kirsch-Darrow L, Fernandez HH, Marsiske M, Okun MS, Bowers D (2006) Dissociating apathy and depression in Parkinson disease. Neurology 67:33–38PubMedCentralCrossRefPubMedGoogle Scholar
  55. 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 17:366–371CrossRefPubMedGoogle Scholar
  56. 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 35:249–255CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Gabriella Santangelo
    • 1
    • 2
  • Paolo Barone
    • 3
  • Sofia Cuoco
    • 1
    • 3
  • Simona Raimo
    • 1
  • Domenica Pezzella
    • 1
  • Marina Picillo
    • 3
  • Roberto Erro
    • 4
    • 5
  • Marcello Moccia
    • 6
  • Maria Teresa Pellecchia
    • 3
  • Marianna Amboni
    • 2
  • Santangelo Franco
    • 6
  • Dario Grossi
    • 1
  • Luigi Trojano
    • 1
    Email author
  • Carmine Vitale
    • 2
    • 7
  1. 1.Department of PsychologySecond University of NaplesCasertaItaly
  2. 2.IDC-Hermitage-CapodimonteNaplesItaly
  3. 3.Department of Medicine and Surgery, Neurodegenerative Diseases CenterUniversity of SalernoSalernoItaly
  4. 4.Dipartimento di Scienze Neurologiche e del MovimentoUniversità di VeronaVeronaItaly
  5. 5.Sobell Department of Motor Neuroscience and Movement DisordersUniversity College London (UCL) Institute of NeurologyLondonUK
  6. 6.Department of Neuroscience Reproductive and Odontostomatologic SciencesUniversity of Naples Federico IINaplesItaly
  7. 7.University ParthenopeNaplesItaly

Personalised recommendations