Please wait a minute...
Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Front. Biol.    2014, Vol. 9 Issue (4) : 324-331    https://doi.org/10.1007/s11515-014-1322-2
RESEARCH ARTICLE
Apathy in Parkinson disease
Marina NODEL1,*(),Nikolay YAKHNO1,Anastasia MEDVEDEVA1,Michail KULIKOV2
1. Sechenov First Moscow State Medical University, Moscow 119991, Russia
2. Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Science, Moscow 117485, Russia
 Download: PDF(150 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

Apathy is one of the least investigated symptom of Parkinson disease (PD). In the article there are data of frequency, diagnostic features, pathophysiology and treatment of apathy in PD. The aim of the investigation was to evaluate the frequency of apathy in PD without dementia, evaluate the relationship with other neuropsychiatric and motor disorders, influence on the life quality. 115 patients (age-63.84±0.6 years, stage-2.6±0.3) with PD without dementia were included in the investigation. There were used the following scales: scale of evaluation stages of PD by Hoehn-Yahr, UPDRS (part ?activity of daily living?, ?motor functions ?); Beck Depression Inventory, Spielberger State Trait Anxiety Inventory, Parkinson Disease Sleep Scale- PDSS, Epworth Sleepiness Scale, Parkinson Fatigue Scale-PFS-16, SCOPA-Cog, Lilli Apathy Rating Scale LARS and Apathy Scale AS.

Apathy was found in 25% of patients. The frequency and severity of apathy does not depend on stage and duration of PD. It was found positive correlation of apathy and hypokinesia. In different stages of PD there was variability of relationships of apathy with depression, executive functions and sleep disorders. We suppose the heterogeneity of apathy in PD because of the variability of the association with other neuropsychiatric (affective, cognitive, sleep) disorders. It was found the negative influence of apathy on daily activity, emotional and social aspects of life quality.

Keywords Parkinson disease      neuropsychiatric symptoms      apathy      heterogeneity     
Corresponding Author(s): Marina NODEL   
Issue Date: 11 August 2014
 Cite this article:   
Marina NODEL,Nikolay YAKHNO,Anastasia MEDVEDEVA, et al. Apathy in Parkinson disease[J]. Front. Biol., 2014, 9(4): 324-331.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-014-1322-2
https://academic.hep.com.cn/fib/EN/Y2014/V9/I4/324
Light degreeModerate degreeSevere degreeTotal
1 stage2114 (13.8%)
2 stage47213 (44.8%)
3 stage2428 (27.6%)
4 stage1124 (13.8%)
Total913729 (100%)
Tab.1  Patients according to the degree of apathy on different stages of PD by LARS scale
LARS interestsLARS novelty seekingLARS motivation- voluntary actionsLARS total scoreAS total score
PDQ- total scorer=0.73, 0.05<p<0.1(1 stage)
PDQ-emotional well-beingr=0.76, p<0.05(1 stage)
PDQ- Stigmar=0.89, p<0.05 (1 stage) n=0.69, 0.05<p<0.1(4 stage)r=0.52, p<0.05(2 stage )
PDQ-cognitionsr=0.75, 0.05<p<0.1(1 stage)r=0.54, p<0.05(2 stage )r=0.52, p<0.05(2 stage)
PDQ-social supportr=0.63, 0.05<p<0.1(4 stage)
PDQ-body discomfortr=0.71, 0.05<p<0.1(1 stage)
UPDRSActivity of daily livingr=0.52, p<0.05(3 stage )r=0.52, p<0.05(2 stage)
Tab.2  The influence of apathy on life quality
Fig.1  The distance between groups is calculated, and does not have interpretive value. Age-the age of onset PD;?Apathy AS-total score AS; Apathy LARS-total LARS score; Executive function-Executive function domain SCOPA- Cog; Cognition-total score SCOPA-Cog ;??Sleep-total score PDSS; Motor functions-part 3 UPDRS , ADL-Activity daily living-part 4 UPDRS; Depression–total score BDI ; Trait Anхiety –score STAI;?Fatigue-mean score PFS-16; Qol-total score PDQ-39.
1 Aarsland D, Larsen J P, Lim N G, Janvin C, Karlsen K, Tandberg E, Cummings J L (1999). Range of neuropsychiatric disturbances in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry, 67(4): 492–496
pmid: 10486397
2 Aarsland D, Mosimann U P, McKeith I G (2000). Role of cholinesterase inhibitors in Parkinsons disease and dementia with Lewy bodies. J Geriatr Psychiatry, 15(5): 387–392
3 Alexander G E, Crutcher M D, DeLong M R (1990). Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Prog Brain Res, 85: 119–146
doi: 10.1016/S0079-6123(08)62678-3 pmid: 2094891
4 Barone P, Antonini A, Colosimo C, Marconi R, Morgante L, Avarello T P, Bottacchi E, Cannas A, Ceravolo G, Ceravolo R, Cicarelli G, Gaglio R M, Giglia R M, Iemolo F, Manfredi M, Meco G, Nicoletti A, Pederzoli M, Petrone A, Pisani A, Pontieri F E, Quatrale R, Ramat S, Scala R, Volpe G, Zappulla S, Bentivoglio A R, Stocchi F, Trianni G, Dotto P D, the PRIAMO study group (2009). The PRIAMO study: A multicenter assessment of nonmotor symptoms and their impact on quality of life in Parkinson’s disease. Mov Disord, 24(11): 1641–1649
doi: 10.1002/mds.22643 pmid: 19514014
5 Beck A T, Streer R A, Brown K G, (1996). Manual for the Beck Depression Inventory –II. San Antonio, TX: Psychological Corporation
6 Benito-León J, Cubo E, Coronell C, the 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(2): 211–218
doi: 10.1002/mds.23872 pmid: 21780179
7 Bogart K R (2011). Is apathy a valid and meaningful symptom or syndrome in Parkinson’s disease? A critical review. Health Psychol, 30(4): 386–400
doi: 10.1037/a0022851 pmid: 21480712
8 Bonelli R M, Cummings J L (2007). Frontal-subcortical circuitry and behavior. Dialogues Clin Neurosci, 9(2): 141–151
pmid: 17726913
9 Aarsland D, Br?nnick K, Alves G, Tysnes O B, Pedersen K F, Ehrt U, Larsen J P (2009). The spectrum of neuropsychiatric symptoms in patients with early untreated Parkinson’s disease. J Neurol Neurosurg Psychiatry, 80(8): 928–930
doi: 10.1136/jnnp.2008.166959 pmid: 19608786
10 Brown R G, Dittner A, Findley L, Wessely S C (2005). The Parkinson fatigue scale. Parkinsonism Relat Disord, 11(1): 49–55
doi: 10.1016/j.parkreldis.2004.07.007 pmid: 15619463
11 Campbell J J, Duffy J D (1997). Treatment strategies in amotivated patients. Psychiatr Ann, 27(1): 44–49
doi: 10.3928/0048-5713-19970101-11
12 Carriere N, Besson P, Dujardin K, Duhamel A, Defebvre L, Delmaire C, Devos D (2014). Apathy in Parkinson’s disease is associated with nucleus accumbens atrophy: A magnetic resonance imaging shape analysis. Mov Disord, 14: 1–7
pmid: 24817690
13 Carver C S, White T L (1994). Behavior inhibition, behavior activation, and affective responses to impending reward and punishment: the BIAS/BAS scales. J Pers Soc Psychol, 67(2): 319–333
doi: 10.1037/0022-3514.67.2.319
14 Cummings J L, Mega M, Gray K, Rosenberg-Thompson S, Carusi D A, Gornbein J (1994). The Neuropsychiatric Inventory: comprehensive assessment of psychopathology in dementia. Neurology, 44(12): 2308–2314
doi: 10.1212/WNL.44.12.2308 pmid: 7991117
15 Chaudhuri K R, Pal S, DiMarco A, Whately-Smith C, Bridgman K, Mathew R, Pezzela F R, Forbes A, H?gl B, Trenkwalder C (2002). The Parkinson’s disease sleep scale: a new instrument for assessing sleep and nocturnal disability in Parkinson’s disease. J Neurol Neurosurg Psychiatry, 73(6): 629–635
doi: 10.1136/jnnp.73.6.629 pmid: 12438461
16 Czernecki V, Schüpbach M, Yaici S, Lévy R, Bardinet E, Yelnik J, Dubois B, Agid Y (2008). Apathy following subthalamic stimulation in Parkinson disease: a dopamine responsive symptom. Mov Disord, 23(7): 964–969
doi: 10.1002/mds.21949 pmid: 18398913
17 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(16): 2391–2397
pmid: 19908317
18 Fahn S, Elton R L, the UPDRS Development Committee(1987). Unified Parkinson’s Disease Rating Scale. In: Fahn S, Marsden C D, Calne D B, Goldstein M, eds. Recent Developments in Parkinson’s Disease. Florham Park, NJ: Macmillan, 153–163
19 Gallagher D A, Lees A J, Schrag A (2010). What are the most important nonmotor symptoms in patients with Parkinson’s disease and are we missing them? Mov Disord, 25(15): 2493–2500
pmid: 20922807
20 Hughes A J, Daniel S E, Kilford L, Lees A J (1992). Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry, 55(3): 181–184
doi: 10.1136/jnnp.55.3.181 pmid: 1564476
21 Johns M W (1991). A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep, 14(6): 540–545
pmid: 1798888
22 Jordan L L, Zahodne L B, Okun M S, Bowers D (2013). Hedonic and behavioral deficits associated with apathy in Parkinson’s disease: potential treatment implications. Mov Disord, 28(9): 1301–1304
doi: 10.1002/mds.25496 pmid: 23712560
23 Kirsch-Darrow L, Fernandez H H, Marsiske M, Okun M S, Bowers D (2006). Dissociating apathy and depression in Parkinson disease. Neurology, 67(1): 33–38
doi: 10.1212/01.wnl.0000230572.07791.22 pmid: 16832074
24 Le Jeune F, Drapier D, Bourguignon A, Péron J, Mesbah H, Drapier S, Sauleau P, Haegelen C, Travers D, Garin E, Malbert C H, Millet B, Vérin M (2009). Subthalamic nucleus stimulation in Parkinson disease induces apathy: a PET study. Neurology, 73(21): 1746–1751
doi: 10.1212/WNL.0b013e3181c34b34 pmid: 19933975
25 Leroi I, David R, Robert P H(2012). Apathy in Parkinsons disease. In: Edmeier K P, Obriien J T, Taylor J-P, eds. Psychiatry of in Parkinsons Disease. Adv Biol Psychiatry. Basel, Karger, 27: 27–40
26 Levy M L, Cummings J L, Fairbanks L A, Masterman D, Miller B L, Craig A H, Paulsen J S, Litvan I (1998). Apathy is not depression. J Neuropsychiatry Clin Neurosci, 10(3): 314–319
pmid: 9706539
27 Levy R, Dubois B (2006). Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cereb Cortex, 16(7): 916–928
doi: 10.1093/cercor/bhj043 pmid: 16207933
28 Marin R S (1990). Differential diagnosis and classification of apathy. Am J Psychiatry, 147(1): 22–30
pmid: 2403472
29 Marin R S, Biedrzycki R C, Firinciogullari S (1991). Reliability and validity of the Apathy Evaluation Scale. Psychiatry Res, 38(2): 143–162
doi: 10.1016/0165-1781(91)90040-V pmid: 1754629
30 Marinus J, Visser M, Verwey N A, Verhey F R J, Middelkoop H A M, Stiggelbout A M, van Hilten J J (2003). Assessment of cognition in Parkinson’s disease. Neurology, 61(9): 1222–1228
doi: 10.1212/01.WNL.0000091864.39702.1C pmid: 14610124
31 Martinez-Martin P, Schapira A H V, Stocchi F, Sethi K, Odin P, MacPhee G, Brown R G, Naidu Y, Clayton L, Abe K, Tsuboi Y, MacMahon D, Barone P, Rabey M, Bonuccelli U, Forbes A, Breen K, Tluk S, Olanow C W, Thomas S, Rye D, Hand A, Williams A J, Ondo W, Chaudhuri K R (2007). Prevalence of nonmotor symptoms in Parkinson’s disease in an international setting; study using nonmotor symptoms questionnaire in 545 patients. Mov Disord, 22(11): 1623–1629
doi: 10.1002/mds.21586 pmid: 17546669
32 McKinlay A, Grace R C, Dalrymple-Alford J C, Anderson T, Fink J, Roger D (2008). A profile of neuropsychiatric problems and their relationship to quality of life for Parkinsons disease. Park Relat Disord, 14: 37–42
33 Mulin E, Leone E, Dujardin K, Delliaux M, Leentjens A, Nobili F, Dessi B, Tible O, Agüera-Ortiz L, Osorio R S, Yessavage J, Dachevsky D, Verhey F R J, Cruz Jentoft A J, Blanc O, Llorca P M, Robert P H (2011). Diagnostic criteria for apathy in clinical practice. Int J Geriatr Psychiatry, 26(2): 158–165
doi: 10.1002/gps.2508 pmid: 20690145
34 Narabayashi H (1999). Akinesia in parkinsonism. In: Joseph A B, Young R R (Eds.). Movement disorders in Neurology and neuropsychiatry. 2nd ed. Oxford: Blackwell Science, 185–188
35 Neugarten B L, Havighurst R J, Tobin S S( 1968). Personality and pattern of aging, in middle age and aging. University of Chicago Press
36 Nodel M R, Yahno N N (2009). Nevropsichiatricheskie zabolevania pri bolezni Parkinsona. Nevrologia. Psihiatria. Psyhosomatika. (Neuropsychiatric disorders in Parkinson disease. Neurology. Neurology. Neuropsychiatry. Psychosomatic), 2: 3–8
37 Nodel M R, Rusakova I M, Yakhno N N(2010). Klinicheskaya otsenka narushenii sna i bodrstvovaniya pri bolezni Parkinsona. Nevrologicheskii zhurnal (Clinical evaluation of sleep and alert disorders in PD. Journal of Neurology-Russian), 2: 19–25
38 Oguru M, Tachibana H, Toda K, Okuda B, Oka N(2010). Apathy and depression in Parkinsons disease. J Geriatric Psych Neurol, 23: 35–41
39 Pedersen K F, Larsen J P, Alves G, Aarsland D (2009). Prevalence and clinical correlates of apathy in Parkinson’s disease: a community-based study. Parkinsonism Relat Disord, 15(4): 295–299
doi: 10.1016/j.parkreldis.2008.07.006 pmid: 18801696
40 Pedersen K F, Alves G, Aarsland D, Larsen J P (2009). Occurrence and risk factors for apathy in Parkinson disease: a 4-year prospective longitudinal study. J Neurol Neurosurg Psychiatry, 80(11): 1279–1282
doi: 10.1136/jnnp.2008.170043 pmid: 19864662
41 Peto V, Jenkinson C, Fitzpatrick R (1998). PDQ-39: a review of the development, validation and application of a Parkinson’s disease quality of life questionnaire and its associated measures. J Neurol, 245(Suppl 1): S10–S14
doi: 10.1007/PL00007730 pmid: 9617716
42 Pluck G C, Brown R G (2002). Apathy in Parkinsons disease. British Medical J, 73: 636–642
43 Postuma R B, Bertrand J A, Montplaisir J, Desjardins C, Vendette M, Rios Romenets S, Panisset M, Gagnon J F (2012). Rapid eye movement sleep behavior disorder and risk of dementia in Parkinson’s disease: a prospective study. Mov Disord, 27(6): 720–726
doi: 10.1002/mds.24939 pmid: 22322798
44 Reijnders J S, Ehrt U, Lousberg R, Aarsland D, Leentjens A F G (2009). The association between motor subtypes and psychopathology in Parkinson’s disease. Parkinsonism Relat Disord, 15(5): 379–382
doi: 10.1016/j.parkreldis.2008.09.003 pmid: 18977165
45 Reijnders J S, Scholtissen B, Weber W E, Aalten P, Verhey F R J, Leentjens A F G (2010). Neuroanatomical correlates of apathy in Parkinson’s disease: A magnetic resonance imaging study using voxel-based morphometry. Mov Disord, 25(14): 2318–2325
doi: 10.1002/mds.23268 pmid: 20669264
46 Remy P, Doder M, Lees A, Turjanski N, Brooks D (2005). Depression in Parkinson’s disease: loss of dopamine and noradrenaline innervation in the limbic system. Brain, 128(Pt 6): 1314–1322
doi: 10.1093/brain/awh445 pmid: 15716302
47 Robbins T W, Everitt B J (1996). Neurobehavioural mechanisms of reward and motivation. Curr Opin Neurobiol, 6(2): 228–236
doi: 10.1016/S0959-4388(96)80077-8 pmid: 8725965
48 Robert P, Onyike C U, Leentjens A F G, Dujardin K, Aalten P, Starkstein S, Verhey F R J, Yessavage J, Clement J P, Drapier D, Bayle F, Benoit M, Boyer P, Lorca P M, Thibaut F, Gauthier S, Grossberg G, Vellas B, Byrne J (2009). Proposed diagnostic criteria for apathy in Alzheimer’s disease and other neuropsychiatric disorders. Eur Psychiatry, 24(2): 98–104
doi: 10.1016/j.eurpsy.2008.09.001 pmid: 19201579
49 Shore D M, Rafal R, Parkinson J A (2011). Appetitive motivational deficits in individuals with Parkinson’s disease. Mov Disord, 26(10): 1887–1892
doi: 10.1002/mds.23736 pmid: 21520287
50 Singer E (1973). Social costs of Parkinson’s disease. J Chronic Dis, 26(4): 243–254
doi: 10.1016/0021-9681(73)90105-7 pmid: 4714571
51 Smith M C, Smith M K, Ellgring H (1996). Spontaneous and posed facial expression in Parkinson’s disease. J Int Neuropsychol Soc, 2(5): 383–391
doi: 10.1017/S1355617700001454 pmid: 9375163
52 Sockeel P, Dujardin K, Devos D, Denève C, Destée A, Defebvre L (2006). The Lille apathy rating scale (LARS), a new instrument for detecting and quantifying apathy: validation in Parkinson’s disease. J Neurol Neurosurg Psychiatry, 77(5): 579–584
doi: 10.1136/jnnp.2005.075929 pmid: 16614016
53 Spielberger C D, Gorsuch R L, Lushene R V (1983). Manual for the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press
54 Starkstein S E, Mayberg H S, Preziosi T J, Andrezejewski P, Leiguarda R, Robinson R G (1992). Reliability, validity, and clinical correlates of apathy in Parkinson’s disease. J Neuropsychiatry Clin Neurosci, 4(2): 134–139
pmid: 1627973
55 Starkstein S E, Jorge R, Mizrahi R, Robinson R G (2006). A prospective longitudinal study of apathy in Alzheimer’s disease. J Neurol Neurosurg Psychiatry, 77(1): 8–11
doi: 10.1136/jnnp.2005.069575 pmid: 16361584
56 Tekin S, Cummings J L (2002). Frontal-subcortical neuronal circuits and clinical neuropsychiatry: an update. J Psychosom Res, 53(2): 647–654
doi: 10.1016/S0022-3999(02)00428-2 pmid: 12169339
57 Thobois S, Lhommée E, Klinger H, Ardouin C, Schmitt E, Bichon A, Kistner A, Castrioto A, Xie J, Fraix V, Pelissier P, Chabardes S, Mertens P, Quesada J L, Bosson J L, Pollak P, Broussolle E, Krack P (2013). Parkinsonian apathy responds to dopaminergic stimulation of D2/D3 receptors with piribedil. Brain, 136(Pt 5): 1568–1577
doi: 10.1093/brain/awt067 pmid: 23543483
58 Vendette M, Gagnon J F, Décary A, (2007). REM sleep behavior disorder predicts cognitive impairment in without dementia. Neurology, 69(19): 1843–1849
doi: 10.1212/01.wnl.0000278114.14096.74 pmid: 17984452
59 Vosnesenskaya T G (2013). The syndrom of apathy. Journal of Neurology-Russian, 3: 4–10
60 Weintraub D, Mavandadi S, Mamikonyan E, Siderowf A D, Duda J E, Hurtig H I, Colcher A, Horn S S, Nazem S, Ten Have T R, Stern M B (2010). Atomoxetine for depression and other neuropsychiatric symptoms in Parkinson disease. Neurology, 75(5): 448–455
doi: 10.1212/WNL.0b013e3181ebdd79 pmid: 20679638
61 Wongpakaran N, van Reekum R, Wongpakaran T, Clarke D (2007). Selective serotonin reuptake inhibitor use associates with apathy among depressed elderly: a case-control study. Ann Gen Psychiatry, 6(1): 7
doi: 10.1186/1744-859X-6-7 pmid: 17313684
[1] Gabrielle Rushing,Rebecca A. Ihrie. Neural stem cell heterogeneity through time and space in the ventricular-subventricular zone[J]. Front. Biol., 2016, 11(4): 261-284.
[2] Haisheng CHEN, Zili SHEN, Zhengxian TONG, Guoshun LIU, . Spatial heterogeneity of available zinc, copper, and manganese in Xiangcheng Tobacco Planting Fields, Henan Province, China[J]. Front. Biol., 2009, 4(4): 469-476.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed