Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-23T08:48:51.678Z Has data issue: false hasContentIssue false

Apathy in patients with Parkinson’s disease following deep brain stimulation of the subthalamic nucleus

Published online by Cambridge University Press:  06 May 2016

Isabel Hindle Fisher
Affiliation:
University of Birmingham Medical School, Birmingham, UK
Hardev S. Pall
Affiliation:
School of Clinical and Experimental Medicine, College of Medicine, University of Birmingham, Birmingham, UK
Rosalind D. Mitchell
Affiliation:
Department of Neurosurgery, Queen Elizabeth Hospital, Birmingham, UK
Jamilla Kausar
Affiliation:
Department of Neurosurgery, Queen Elizabeth Hospital, Birmingham, UK
Andrea E. Cavanna*
Affiliation:
School of Clinical and Experimental Medicine, College of Medicine, University of Birmingham, Birmingham, UK Department of Neuropsychiatry, Birmingham and Solihull Mental Health NHS Foundation Trust, Birmingham, UK School of Life and Health Sciences, Aston University, Birmingham, UK
*
*Address for correspondence: Andrea E. Cavanna, MD, PhD, FRCP, Department of Neuropsychiatry, The Barberry National Centre for Mental Health, Birmingham B15 2FG, United Kingdom. (Email: a.e.cavanna@bham.ac.uk)

Abstract

Objective

Apathy has been reported as a possible adverse effect of deep brain stimulation of the subthalamic nucleus (STN-DBS). We investigated the prevalence and severity of apathy in 22 patients with Parkinson’s disease (PD) who underwent STN-DBS, as well as the effects of apathy on quality of life (QOL).

Methods

All patients were assessed with the Lille Apathy Rating Scale (LARS), the Apathy Scale (AS), and the Parkinson’s Disease Questionnaire and were compared to a control group of 38 patients on pharmacotherapy alone.

Results

There were no significant differences in the prevalence or severity of apathy between patients who had undergone STN-DBS and those on pharmacotherapy alone. Significant correlations were observed between poorer QOL and degree of apathy, as measured by the LARS (p<0.001) and the AS (p=0.021). PD-related disability also correlated with both apathy ratings (p<0.001 and p=0.017, respectively).

Conclusion

Our findings suggest that STN-DBS is not necessarily associated with apathy in the PD population; however, more severe apathy appears to be associated with a higher level of disability due to PD and worse QOL, but no other clinico-demographic characteristics.

Type
Original Research
Copyright
© Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

The authors would like to thank all the participants who gave up their time to take part in this study. Gratitude is also expressed to Mrs. Lesley Roberts for support during the development and write-up of this project, and to Mr Sayeed Haque, Mr. Roger Holder, and Mrs. Andrea Roalfe for their help with the statistical analyses.

The abstract of the present article was presented at the XXVII British Neuropsychiatry Association Annual General Meeting, London, February 4–6, 2015.

References

1. Leroi, I, David, A, Robert, P. Apathy in Parkinson’s disease. In: Ebmeier KP, O’Brian JT, Taylor JP, eds. Psychiatry of Parkinson’s Disease: Advances in Biological Psychiatry. Basel: Karger; 2012: 2740.CrossRefGoogle Scholar
2. Benoit, M, Andrieu, S, Lechowski, L. Apathy and depression in Alzheimer’s disease are associated with functional deficit and psychotropic prescription. Int J Geriatr Psychiatry. 2008; 23(4): 409414.Google Scholar
3. Diamond, A, Jankovic, J. The effect of deep brain stimulation on quality of life in movement disorders. J Neurol Neurosurg Psychiatry. 2005; 76(9): 11881193.CrossRefGoogle ScholarPubMed
4. Barone, P, Antonini, A, Colosimo, C, et al. The PRIAMO study: a multicenter assessment of nonmotor symptoms and their impact on quality of life in Parkinson’s disease. Mov Disord. 2009; 24(11): 16411649.CrossRefGoogle ScholarPubMed
5. Ceravolo, R, Pagni, C, Tognoni, G, Bonuccelli, U. The epidemiology and clinical manifestations of dysexecutive syndrome in Parkinson’s disease. Front Neurol. 2012; 3: 159.CrossRefGoogle ScholarPubMed
6. Antonini, A, Barone, P, Marconi, R, et al. The progression of non-motor symptoms in Parkinson’s disease and their contribution to motor disability and quality of life. J Neurol. 2012; 259(12): 26212631.Google Scholar
7. Thobois, S, Ardouin, C, Lhommée, E, et al. Non-motor dopamine withdrawal syndrome after surgery for Parkinson’s disease: predictors and underlying mesolimbic denervation. Brain. 2010; 133(Pt 4): 11111127.CrossRefGoogle ScholarPubMed
8. Funkiewiez, A, Ardouin, C, Caputo, E, et al. Long term effects of bilateral subthalamic nucleus stimulation on cognitive function, mood, and behaviour in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2004; 75(6): 834839.CrossRefGoogle ScholarPubMed
9. Kirsch-Darrow, L, Zahodne, L, Marsiske, M, Okun, MS, Foote, KD, Bowers, D. The trajectory of apathy after deep brain stimulation: from pre-surgery to 6 months post-surgery in Parkinson’s disease. Parkinsonism Relat Disord. 2011; 17(3): 182188.Google Scholar
10. Drapier, D, Drapier, S, Sauleau, P, et al. Does subthalamic nucleus stimulation induce apathy in Parkinson’s disease? J Neurol. 2006; 253(8): 10831091.CrossRefGoogle ScholarPubMed
11. Denheyer, M, Kiss, Z, Haffenden, A. Behavioral effects of subthalamic deep brain stimulation in Parkinson’s disease. Neuropsychologia. 2009; 47(14): 32033209.Google Scholar
12. Porat, O, Cohen, O, Schwartz, R, Hassin-Baer, S. Association of preoperative symptom profile with psychiatric symptoms following subthalamic nucleus stimulation in patients with Parkinson’s disease. J Neuropsychiatry Clin Neurosci. 2009; 21(4): 398405.CrossRefGoogle ScholarPubMed
13. Saint-Cyr, J, Trepanier, L, Kumar, R, Lozano, AM, Lang, AE. Neuropsychological consequences of chronic bilateral stimulation of the subthalamic nucleus in Parkinson’s disease. Brain. 2000; 123(Pt 10): 20912108.CrossRefGoogle ScholarPubMed
14. Drapier, D, Péron, J, Leray, E, et al. Emotion recognition impairment and apathy after subthalamic nucleus stimulation in Parkinson’s disease have separate neural substrates. Neuropsychologia. 2008; 46(11): 27962801.CrossRefGoogle ScholarPubMed
15. Le Jeune, F, Drapier, D, Bourguignon, A, et al. Subthalamic nucleus stimulation in Parkinson disease induces apathy: a PET study. Neurology. 2009; 73(21): 17461751.Google Scholar
16. Funkiewiez, A, Ardouin, C, Cools, R, et al. Effects of levodopa and subthalamic nucleus stimulation on cognitive and affective functioning in Parkinson’s disease. Mov Disord. 2006; 21(10): 16561662.Google Scholar
17. Krack, P, Batir, A, Van Blercom, N, et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med. 2003; 349(20): 19251934.Google Scholar
18. Campbell, M, Black, K, Weaver, P, et al. Mood response to deep brain stimulation of the subthalamic nucleus in Parkinson’s disease. J Neuropsychiatry Clin Neurosci. 2012; 24(1): 2836.Google Scholar
19. Czernecki, V, Pillon, B, Houeto, J, et al. Does bilateral high-frequency stimulation of the subthalamic nucleus aggravate apathy in Parkinson’s disease? J Neurol Neurosurg Psychiatry. 2005; 76(6): 775779.Google Scholar
20. Castelli, L, Lanotte, M, Zibetti, M, et al. Apathy and verbal fluency in STN-stimulated PD patients: an observational follow-up study. J Neurol. 2007; 254(9): 12381243.CrossRefGoogle ScholarPubMed
21. Castelli, L, Perozzo, P, Zibetti, M, et al. Chronic deep brain stimulation of the subthalamic nucleus for Parkinson’s disease: effects on cognition, mood, anxiety and personality traits. Eur Neurol. 2006; 55(3): 136144.Google Scholar
22. Chou, L, Persad, C, Patil, P. Change in fatigue after bilateral subthalamic nucleus deep brain stimulation for Parkinson’s disease. Parkinsonism Relat Disord. 2012; 18(5): 510513.Google Scholar
24. Tomlinson, C, Stowe, R, Patel, S, Rick, C, Gray, R, Clarke, CE. Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord. 2010; 25(15): 26492653.Google Scholar
25. Leentjens, A, Dujardin, K, Marsh, L. Apathy and anhedonia rating scales in Parkinson’s disease: critique and recommendations. Mov Disord. 2008; 23(14): 20042013.Google Scholar
26. The Movement Disorder Society Rating Scales. http://www.movementdisorders.org/publications/rating_scales/. Accessed August 11, 2014.Google Scholar
27. Drijgers, R, Dujardin, K, Reijnders, J, Defebvre, L, Leentjens, AF. Validation of diagnostic criteria for apathy in Parkinson’s disease. Parkinsonism Relat Disord. 2010; 16(10): 656660.Google Scholar
28. Zahodne, L, Young, S, Kirsch-Darrow, L, et al. Examination of the Lille Apathy Rating Scale in Parkinson disease. Mov Disord. 2009; 24(5): 677683.CrossRefGoogle ScholarPubMed
29. Peto, V, Jenkinson, C, Fitzpatrick, R, Greenhall, R. The development and validation of a short measure of functioning and well being for individuals with Parkinson’s disease. Qual Life Res. 1995; 4(3): 241248.Google Scholar
30. Kirsch-Darrow, L, Zahodne, L, Hass, C, et al. How cautious should we be when assessing apathy with the Unified Parkinson’s Disease Rating Scale? Mov Disord. 2009; 24(5): 684688.Google Scholar
31. Weaver, F, Follett, K, Stern, M, et al. Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease. JAMA. 2009; 301(1): 6373.CrossRefGoogle ScholarPubMed
32. Kleiner-Fisman, G, Stern, M, Fisman, D. Health-related quality of life in Parkinson disease: correlation between Health Utilities Index III and Unified Parkinson’s Disease Rating Scale (UPDRS) in U.S. male veterans. Health Qual Life Outcomes. 2010; 8: 91.Google Scholar
33. Lyons, K, Pahwa, R. Long-term benefits in quality of life provided by bilateral subthalamic stimulation in patients with Parkinson disease. J Neurosurg. 2005; 103(2): 252255.Google Scholar
34. Soha, S, Morrisa, M, McGinley, J. Determinants of health-related quality of life in Parkinson’s disease: a systematic review. Parkinsonism Relat Disord. 2011; 17(1): 19.Google Scholar
35. Pederson, A, Alves, G, Brønnick, K, Aarsland, D, Tysnes, OB, Larsen, JP. Apathy in drug-naive patients with incident Parkinson’s disease: the Norwegian Park West study. J Neurol. 2010; 257(2): 217223.Google Scholar
36. Cubo, E, Benito-León, J, Coronell, C, Armesto, D, ANIMO Study Group. Clinical correlates of apathy in patients recently diagnosed with Parkinson’s disease: the ANIMO study. Neuroepidemiology. 2012; 38(1): 4855.Google Scholar
37. Pederson, K, Larsen, J, Alves, G, Aarsland, D. Prevalence and clinical correlates of apathy in Parkinson’s disease: a community-based study. Parkinsonism Relat Disord. 2009; 15(4): 295299.Google Scholar
38. Robert, G, Le Jeune, F, Lozachmeur, C, et al. Apathy in patients with Parkinson disease without dementia or depression: a PET study. Neurology. 2012; 79(11): 11551160.CrossRefGoogle ScholarPubMed
39. Higuchi, MA, Tsuboi, Y, Inoue, T, et al. Predictors of the emergence of apathy after bilateral stimulation of the subthalamic nucleus in patients with Parkinson’s disease. Neuromodulation. 2015; 18(2): 113117.Google Scholar
40. Kirsch-Darrow, L, Marsiske, M, Okun, M, Bauer, R, Bowers, D. Apathy and depression: separate factors in Parkinson’s disease. J Int Neuropsychol Soc. 2011; 17(6): 10581066.CrossRefGoogle ScholarPubMed
41. Czernecki, V, Pillon, B, Houeto, J, Pochon, JB, Levy, R, Dubois, B. Motivation, reward, and Parkinson’s disease: influence of dopatherapy. Neuropsychologia. 2002; 40(13): 22572267.CrossRefGoogle ScholarPubMed
42. Lozachmeur, C, Drapier, S, Robert, G, et al. Pallidal stimulation in Parkinson’s disease does not induce apathy. J Neuropsychiatry Clin Neurosci. 2014; 26(3): 221226.Google Scholar
43. Martinez-Fernandez, R, Pelissier, P, Quesada, JL, et al. Postoperative apathy can neutralise benefits in quality of life after subthalamic stimulation for Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2016; 87: 311318.Google Scholar