Advertisement

Clinical and demographic correlates of apathy in Parkinson’s disease

  • Daniel S. Brown
  • Matthew J. Barrett
  • Joseph L. Flanigan
  • Scott A. Sperling
Original Communication

Abstract

Objective

To better understand the demographic, neuropsychiatric, cognitive, and motor predictors of apathy in Parkinson’s disease (PD).

Method

112 participants (Mage = 68.53 years; Mdisease duration = 6.17 years) were administered the Apathy Scale (AS), Beck Depression Inventory-II (BDI-II), Movement Disorder Society Unified Parkinson’s Disease Rating Scale (MDS-UPDRS), Trail Making Test (TMT), Wechsler Adult Intelligence Scale-IV Matrix Reasoning subtest, letter (F-A-S) and category (Animals) fluency, and Hopkins Verbal Learning Test-Revised. Psychosis was assessed. A stepwise logistic regression analysis was performed to investigate the ability of demographic factors and clinical assessments to predict nonapathetic (AS ≤ 13) versus apathetic (AS > 13) group membership.

Results

The regression analysis yielded a robust model in which older age, less education, elevated BDI-II, current psychosis, higher MDS-UPDRS Part III (motor score), and slower TMT-B performance predicted membership in the apathetic group, with a correct classification rate of 77.5% (Nagelkerke R2 = 0.48, p < .001). Depression (OR = 9.20, p < .001) and education (OR = 0.66, p = 0.002) contributed significantly to the overall model. A linear regression with AS score as the outcome variable was similar, but TMT-B additionally contributed significantly (p = 0.02) to the overall model, F(6, 86) = 12.02, p < .001, adjusted R2 = 0.42.

Conclusions

Of the factors examined, depression, education, and executive functioning were the strongest correlates of apathy in PD. These results support the idea that common underlying frontosubcortical disruptions in this population contribute to apathy, depression, and executive dysfunction.

Keywords

Parkinson’s disease Apathy Depression Cognition Executive function 

Notes

Acknowledgements

This study was funded by the American Parkinson Disease Association Center for Advanced Research at the University of Virginia.

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflict of interest.

Ethical standards

This study received local institutional review board approval and has, therefore, been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

Informed consent

Written informed consent was obtained from all participants prior to their inclusion in the study.

References

  1. 1.
    Bernal-Pacheco O, Fernandez HH (2013) Apathy in Parkinson’s disease. In: Pfeiffer RR, Bodis-Wollner I (eds) Parkinson’s disease and nonmotor dysfunction, 2nd edn. Humana Press, Totowa, pp 119–129CrossRefGoogle Scholar
  2. 2.
    Thant T, Yager J (2018) Updating apathy: using research domain criteria to inform clinical assessment and diagnosis of disorders of motivation. J Nerv Ment Dis Advance on.  https://doi.org/10.1097/NMD.0000000000000860 CrossRefGoogle Scholar
  3. 3.
    Aarsland D, Marsh L, Schrag A (2009) Neuropsychiatric symptoms in Parkinson’s disease. Mov Disord 24:2175–2186.  https://doi.org/10.1002/mds.22589 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Pagonabarraga J, Kulisevsky J, Strafella AP, Krack P (2015) Apathy in Parkinson’s disease: Clinical features, neural substrates, diagnosis, and treatment. Lancet Neurol 14:518–531.  https://doi.org/10.1016/S1474-4422(15)00019-8 CrossRefPubMedGoogle Scholar
  5. 5.
    Bogart KR (2011) Is apathy a valid and meaningful symptom or syndrome in Parkinson’s disease? A critical review. Heal Psychol 30:386–400.  https://doi.org/10.1037/a0022851 CrossRefGoogle Scholar
  6. 6.
    Leroi I, Harbishettar V, Andrews M et al (2012) Carer burden in apathy and impulse control disorders in Parkinson’s disease. Int J Geriatr Psychiatry 27:160–166.  https://doi.org/10.1002/gps.2704 CrossRefPubMedGoogle Scholar
  7. 7.
    Starkstein SE, Brockman S (2011) Apathy and Parkinson’s disease. Curr Treat Options Neurol 13:267–273.  https://doi.org/10.1007/s11940-011-0118-9 CrossRefPubMedGoogle Scholar
  8. 8.
    Isella V, Melzi P, Grimaldi M et al (2002) Clinical, neuropsychological, and morphometric correlates of apathy in Parkinson’s disease. Mov Disord 17:366–371.  https://doi.org/10.1002/mds.10041 CrossRefPubMedGoogle Scholar
  9. 9.
    Leroi I, David R, Robert PH (2012) Apathy in Parkinson’s disease. In: Ebmeier KP, O’Brien JT, Taylor J-P (eds) Psychiatry of Parkinson’s disease. Karger, Basel, pp 27–40CrossRefGoogle Scholar
  10. 10.
    Levy R, Dubois B (2006) Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cereb Cortex 16:916–928.  https://doi.org/10.1093/cercor/bhj043 CrossRefPubMedGoogle Scholar
  11. 11.
    García-Ramos R, Villanueva C, del Val J, Matías-Guíu J (2010) Apathy in Parkinson’s disease. Neurología 25:40–50.  https://doi.org/10.1016/S0213-4853(10)70021-9 CrossRefPubMedGoogle Scholar
  12. 12.
    Santangelo G, Trojano L, Barone P et al (2013) Apathy in Parkinson’s disease: Diagnosis, neuropsychological correlates, pathophysiology and treatment. Behav Neurol 27:501–513.  https://doi.org/10.3233/BEN-129025 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Benito-León J, Cubo E, Coronell C (2012) Impact of apathy on health-related quality of life in recently diagnosed Parkinson’s disease: the ANIMO study. Mov Disord 27:211–218.  https://doi.org/10.1002/mds.23872 CrossRefPubMedGoogle Scholar
  14. 14.
    Cubo E, Benito-León J, Coronell C, Armesto D (2012) Clinical correlates of apathy in patients recently diagnosed with Parkinson’s disease: the ANIMO Study. Neuroepidemiology 38:48–55.  https://doi.org/10.1159/000334314 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Pedersen KF, Larsen JP, Alves G, Aarsland D (2009) Prevalence and clinical correlates of apathy in Parkinson’s disease: a Community-based study. Park Relat Disord 15:295–299.  https://doi.org/10.1016/j.parkreldis.2008.07.006 CrossRefGoogle Scholar
  16. 16.
    Dujardin K, Sockeel P, Delliaux M et al (2009) Apathy may herald cognitive decline and dementia in Parkinson’s disease. Mov Disord 24:2391–2397.  https://doi.org/10.1002/mds.22843 CrossRefPubMedGoogle Scholar
  17. 17.
    Oguru M, Tachibana H, Toda K et al (2010) Apathy and depression in Parkinson disease. J Geriatr Psychiatry Neurol 23:35–41.  https://doi.org/10.1177/0891988709351834 CrossRefPubMedGoogle Scholar
  18. 18.
    Skorvanek M, Rosenberger J, Gdovinova Z et al (2013) Apathy in elderly nondemented patients with Parkinson’s disease: clinical determinants and relationship to quality of life. J Geriatr Psychiatry Neurol 26:237–243.  https://doi.org/10.1177/0891988713500587 CrossRefPubMedGoogle Scholar
  19. 19.
    Dujardin K, Sockeel P, Devos D et al (2007) Characteristics of apathy in Parkinson’s disease. Mov Disord 22:778–784.  https://doi.org/10.1002/mds.21316 CrossRefPubMedGoogle Scholar
  20. 20.
    Martínez-Horta S, Pagonabarraga J, Fernández de Bobadilla R et al (2013) Apathy in Parkinson’s disease: more than just executive dysfunction. J Int Neuropsychol Soc 19:571–582.  https://doi.org/10.1017/S1355617713000131 CrossRefPubMedGoogle Scholar
  21. 21.
    Meyer A, Zimmermann R, Gschwandtner U et al (2015) Apathy in Parkinson’s disease is related to executive function, gender and age but not to depression. Front Aging Neurosci 6:1–6.  https://doi.org/10.3389/fnagi.2014.00350 CrossRefGoogle Scholar
  22. 22.
    Pluck GC, Brown RG (2002) Apathy in Parkinson’s disease. J Neurol Neurosurg Psychiatry 73:636–642.  https://doi.org/10.1136/jnnp.73.6.636 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    den Brok MGHE, van Dalen JW, van Gool WA et al (2015) Apathy in Parkinson’s disease: a systematic review and meta-analysis. Mov Disord 30:759–769.  https://doi.org/10.1002/mds.26208 CrossRefGoogle Scholar
  24. 24.
    Gibb WRG, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 51:745–752.  https://doi.org/10.1136/jnnp.51.6.745 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Emre M, Aarsland D, Brown R et al (2007) Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 22:1689–1707.  https://doi.org/10.1002/mds.21507 CrossRefPubMedGoogle Scholar
  26. 26.
    Goetz CG, Poewe W, Rascol O et al (2004) Movement Disorder Society Task Force report on the Hoehn and Yahr staging scale: status and recommendations. Mov Disord 19:1020–1028.  https://doi.org/10.1002/mds.20213 CrossRefPubMedGoogle Scholar
  27. 27.
    Tomlinson CL, Stowe R, Patel S et al (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25:2649–2653.  https://doi.org/10.1002/mds.23429 CrossRefPubMedGoogle Scholar
  28. 28.
    Starkstein SE, Mayberg HS, Preziosi TJ et al (1992) Reliability, validity, and clinical correlates of apathy in Parkinson’s disease. J Neuropsychiatry Clin Neurosci 4:134–139.  https://doi.org/10.1176/jnp.4.2.134 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Marin RS, Biedrzycki RC, Firinciogullari S (1991) Reliability and validity of the Apathy Evaluation Scale. Psychiatry Res 38:143–162.  https://doi.org/10.1016/0165-1781(91)90040-V CrossRefPubMedGoogle Scholar
  30. 30.
    Leentjens AFG, Dujardin K, Marsh L et al (2008) Apathy and anhedonia rating scales in Parkinson’s disease: critique and recommendations. Mov Disord 23:2004–2014.  https://doi.org/10.1002/mds.22229 CrossRefPubMedGoogle Scholar
  31. 31.
    Beck AT, Steer RA, Brown GK (1996) Manual for the beck depression inventory-II. Psychological Corporation, San AntonioGoogle Scholar
  32. 32.
    Grace J, Malloy PF (2001) Frontal systems behvaior scale: professional manual. Psychological Assessment Resources, Inc., LutzGoogle Scholar
  33. 33.
    Ravina B, Marder K, Fernandez HH et al (2007) Diagnostic criteria for psychosis in Parkinson’s disease: Report of an NINDS, NIMH Work Group. Mov Disord 22:1061–1068.  https://doi.org/10.1002/mds.21382 CrossRefPubMedGoogle Scholar
  34. 34.
    Goetz CG, Tilley BC, Shaftman SR et al (2008) Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): Scale presentation and clinimetric testing results. Mov Disord 23:2129–2170.  https://doi.org/10.1002/mds.22340 CrossRefPubMedGoogle Scholar
  35. 35.
    Nasreddine ZS, Phillips NA, Bédirian V et al (2005) The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53:695–699.  https://doi.org/10.1111/j.1532-5415.2005.53221.x CrossRefPubMedGoogle Scholar
  36. 36.
    Brown DS, Bernstein IH, McClintock SM et al (2016) Use of the Montreal Cognitive Assessment and Alzheimer’s Disease-8 as cognitive screening measures in Parkinson’s disease. Int J Geriatr Psychiatry 31:264–272.  https://doi.org/10.1002/gps.4320 CrossRefPubMedGoogle Scholar
  37. 37.
    Reitan R, Wolfson D (1985) The Halstead-Reitan Neuropsychological Test Battery. Neuropsychological Publishing Group, TucsonGoogle Scholar
  38. 38.
    Wechsler D (2008) Wechsler Adult Intelligence Scale-Fourth Edition. Pearson Education, Inc., San AntonioGoogle Scholar
  39. 39.
    Lezak MD, Howieson DB, Bigler ED, Tranel D (2012) Neuropsychological assessment, 5th edn. Oxford University Press, Inc., New YorkGoogle Scholar
  40. 40.
    Strauss E, Sherman EMS, Spreen O (2006) A compendium of neuropsychological tests: administration, norms, and commentary, 3rd edn. Oxford University Press, Inc., New YorkGoogle Scholar
  41. 41.
    Brandt J, Benedict RHB (2001) Hopkins verbal learning test-revised: professional manual. Psychological Assessment Resources, Inc., LutzGoogle Scholar
  42. 42.
    Heaton RK, Miller SW, Taylor MJ, Grant I (2004) Revised comprehensive norms for an expanded Halstead-Reitan battery: demographically adjusted neuropsychological norms for African American and Caucasian adults. Psychological Assessment Resources, Inc., LutzGoogle Scholar
  43. 43.
    Dalrymple-Alford JC, MacAskill MR, Nakas CT et al (2010) The MoCA: Well-suited screen for cognitive impairment in Parkinson disease. Neurology 75:1717–1725.  https://doi.org/10.1212/WNL.0b013e3181fc29c9 CrossRefGoogle Scholar
  44. 44.
    Hoops S, Nazem S, Siderowf a D et al (2009) Validity of the MoCA and MMSE in the detection of MCI and dementia in Parkinson disease. Neurology 73:1738–1745.  https://doi.org/10.1212/WNL.0b013e3181c34b47 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    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.  https://doi.org/10.1097/WNN.0b013e318145a6f6 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Arbuthnott K, Frank J (2000) Trail Making Test, Part B as a measure of executive control: Validation using a set-switching paradigm. J Clin Exp Neuropsychol 22:518–528.  https://doi.org/10.1076/1380-3395(200008)22:4;1-0;FT518 CrossRefPubMedGoogle Scholar
  47. 47.
    Muslimovic D, Post B, Speelman JD, Schmand B (2005) Cognitive profile of patients with newly diagnosed Parkinson disease. Neurology 65:1239–1245.  https://doi.org/10.1212/01.wnl.0000180516.69442.95 CrossRefPubMedGoogle Scholar
  48. 48.
    Zgaljardic DJ, Foldi NS, Borod JC (2004) Cognitive and behavioral dysfunction in Parkinson’s disease: neurochemical and clinicopathological contributions. J Neural Transm 111:1287–1301.  https://doi.org/10.1007/s00702-004-0178-z CrossRefPubMedGoogle Scholar
  49. 49.
    Lorant V, Deliège D, Eaton W et al (2003) Socioeconomic inequalities in depression: a meta-analysis. Am J Epidemiol 157:98–112.  https://doi.org/10.1093/aje/kwf182 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of NeurologyUniversity of VirginiaCharlottesvilleUSA

Personalised recommendations