Empathy In Neurodegenerative Diseases: A Systematic Review

Figures & data

Table 1 Summary Of Eligibility And Inclusion Criteria

Eligibility Criteria
From January 1, 1988 to July 31, 2019
Original research articles
Written in English
Published in international peer-reviewed journals
Inclusion criteria
Assessing adult patients
Empathy assessed through quantitative measures
Comparison with a healthy control group
Cross-sectional study

Figure 1 Flow diagram for qualitative systematic review of empathy functioning in neurodegenerative diseases.

Table 2 Summary Of The Number Of Articles Retrieved For Each Source Of Information, For Each Disease

	Database	Scopus	PubMed	PsycINFO	External Sources	Total	Used
Disease
Alzheimer's disease		221	19	22	0	262	8
Frontotemporal dementia		192	71	57	1	321	14
Dementia of Lewy bodies		14	2	2	0	18	0
Parkinson's disease		71	12	10	0	93	2
Prion disease		1	0	0	0	1	0
Huntington's disease		24	11	8	0	43	6
Chorea minor		0	0	0	0	0	0
Ataxias		11	1	1	0	13	0
Amyotrophic lateral sclerosis		50	12	2	0	64	3
Primary lateral sclerosis		7	0	0	0	7	0
Hereditary spastic paraparesis		0	0	0	0	0	0
Spinal and bulbar muscular atrophy		1	1	0	1	3	2
Myotonic dystrophy		2	1	0	1	4	2
Total		594	130	102	3	829	37

Table 3 Review Results Sorted By Disease

References	Participants	Type Of Empathy	Methods		Results (“<” Lower Than Controls; “=” Equals To Controls; “>” Greater Than Controls)
			Empathy evaluation	Cognitive deficits	Affective empathy	Cognitive empathy	Affective mentalizing	Cognitive mentalizing
AD only
Sturm et al, 2013^Citation36	64 AD, 62 MCI and 111 HC	Affective empathy	IRI other-rated	AD yes; MCI no	<	NA	NA	NA
Nash et al, 2007^Citation38	20 AD and 20 HC	Cognitive and affective empathy	IRI self-rated	Yes	=	<	NA	NA
Lee et al, 2013^Citation42	12 AD, all females, and 12 HC	Affective mentalizing	Facial emotion recognition	Yes	NA	NA	=	NA
AD and FTD
Fernandez-Duque et al, 2010^Citation34	8 AD, 9 bvFTD and 10 HC	Cognitive and affective empathy	Videotape for inference on thoughts and feelings, IRI other-rated	Yes	< (only for ambivalent video); IRI: bvFTD < AD	< (only for ambivalent video); IRI: bvFTD < AD	NA	NA
Narme et al, 2013^Citation35	13 AD, 13 FTLD (bvFTD and SD) and 26 HC	Cognitive and affective empathy. Cognitive and affective mentalizing	IRI other-rated, Ekman 60, FPT, Yoni task	Yes	FTLD < AD < HC	FTLD < AD < HC	Ekman 60 (FTLD < AD; AD = HC); FPT (FTLD < HC); Yoni (FTLD & AD < HC)	FPT (FTLD & AD < HC); Yoni (FTLD & AD = HC)
Dermody et al, 2016^Citation37	25 AD, 24 bvFTD and 22 HC	Cognitive and affective empathy. Affective mentalizing	Ekman 60, IRI other-rated	Yes	AD =; bvFTD <	AD <; bvFTD <	AD =; bvFTD <	NA
Rankin et al, 2005^Citation39	16 AD, 37 FTLD (18 bvFTD and 19 SD) and 10 HC	Cognitive and affective empathy	IRI other-rated	Yes	AD =; bvFTD =; SD <	AD =; bvFTD <; SD <	NA	NA
AD and PD
Martinez et al, 2018^Citation44	25 AD, 17 PD and 42 HC	Cognitive and affective empathy. Affective mentalizing	EET of TASIT, IRI other-rated	Yes	NA	NA	<	NA
FTD only
Lough et al, 2006^Citation51	18 bvFTD and 13 HC	Cognitive and affective empathy. Affective mentalizing	Four mentalizing tasks, facial emotion recognition, IRI other-rated	Yes	<	<	<	NA
Hua et al, 2018^Citation52	26 bvFTD and 25 HC	Cognitive and affective empathy. Emotional contagion. Affective mentalizing	Emotion recognition task, IRI other-rated for patients and controls	Yes	<	<	<	NA
Eslinger et al, 2011^Citation53	12 bvFTD, 7 PNFA, 7 SD and 16 HC	Cognitive and affective empathy	IRI	Not reported	Self-rating =; Other-rating bvFTD <; PNFA =; SD =	Self-rating =; Other-rating bvFTD <; PNFA =; SD =	NA	NA
Eslinger et al, 2007^Citation54	26 FTD (12 SOC/EXEC and 14 APH) and 17 HC	Cognitive and affective empathy	GCPT, Happé, empathy questionnaire (self- and other-rated)	Yes	Self-rating =; Other-rating <; Other-rating OSC/EXEC < APH	Self-rating =; Other-rating <	NA	NA
Baez et al, 2014^Citation55	37 bvFTD and 30 HC	Cognitive and affective empathy. Affective mentalizing	EPT, EET of TASIT, RMET	Yes	<	<	<	NA
Cerami et al, 2014^Citation56	18 bvFTD and 36 HC	Cognitive and affective mentalizing	SET	Yes	NA	NA	<	<
Caminiti et al, 2015^Citation57	12 bvFTD and 30 HC	Cognitive and affective mentalizing	SET	Yes	NA	NA	<	<
Kamminga et al, 2015^Citation58	19 bvFTD, 12 right-damaged SD and 20 HC	Affective mentalizing	Three tasks on facial emotion recognition	Yes	NA	NA	<	NA
Baez et al, 2016^Citation59	26 bvFTD and 23 HC	Cognitive and affective empathy	EPT	Yes	<	<	NA	NA
Oliver et al, 2015^Citation60	24 bvFTD and 24 HC	Cognitive and affective empathy	MET	Yes	<	<	NA	NA
PD only
Narme et al, 2013^Citation63	23 non-demented PD and 46 HC	Cognitive and affective empathy. Cognitive and affective mentalizing	IRI other-rated, Ekman 60, FPT, Yoni task	Yes	<	<	<	<
HD only
Trinkler et al, 2013^Citation82	13 HD and 13 HC	Cognitive and affective empathy. Affective mentalizing	Facial emotion recognition (Ekman and Lundqvist), facial emotion expression (mimic), IRI and BEES self-rated	Yes	=	=	<	NA
Adjeroud et al, 2016^Citation83	23 manifest HD, 16 preclinical HD and 39 HC	Cognitive and affective empathy. Cognitive and affective mentalizing	Yoni test, self-rated IRI and BES	Manifest HD = Yes Preclinical HD = No	Manifest =; Preclinical =	Manifest =; Preclinical =	Manifest <; Preclinical =	Manifest <; Preclinical =
Maurage et al, 2016^Citation84	19 manifest HD, 17 preclinical HD and 36 HC	Cognitive and affective empathy	EQ self-rated	Yes	Manifest =; Preclinical =	Manifest <; Preclinical =	NA	NA
Eddy et al, 2015^Citation85	20 preclinical HD and 26 HC	Cognitive and affective empathy. Affective mentalizing	FPT, RMET, IRI	No	=	<	<	NA
Baez et al, 2015^Citation86	18 manifest HD, 19 relatives w/out genetic testing and 36 HC	Cognitive and affective empathy. Affective mentalizing	EPT, EET of TASIT, ad-hoc emotion recognition	Manifest HD = Yes Relatives = No	Manifest =; relatives =	Manifest <; relatives =	Manifest =; relatives =	NA
Trinkler et al, 2017^Citation87	28 HD and 24 HC	Emotional contagion, affective mentalizing	Facial emotion recognition (Ekman and Lundqvist)	Yes	<	NA	<	NA
ALS only
Cerami et al, 2014^Citation95	20 non-demented ALS (4 cognitively and 2 behaviorally impaired), 56 HC	Cognitive and affective mentalizing	SET	80% no; 20% yes	NA	<	<	=
van der Hulst et al, 2015^Citation96	33 non-demented ALS and 26 HC	Cognitive and affective empathy. Cognitive and affective mentalizing	Cognitive–Affective Judgement of Preference Test (similar to Yoni), IRI self- or other-rated	Yes for verbal tests, no for spatial tests	=	=	<	=
Watermeyer et al, 2015^Citation97	55 non-FTD-demented ALS and 49 HC	Cognitive and affective empathy. Affective mentalizing	RMET, TASIT, Happé, IRI	Yes, but normal IQ	IRI =	IRI =; Happé <	=	NA
SBMA only
Di Rosa et al, 2015^Citation102	20 SBMA and 18 HC	Cognitive empathy and affective mentalizing	FPT, RMET	No	NA	<	=	NA
Marcato et al, 2018^Citation103	64 SBMA and 78 HC	Affective empathy	Story with affective valence	No	>	NA	NA	NA
DM1 only
Labaryu et al, 2018^Citation123	38 DM1 and 38 HC	Cognitive and affective empathy. Affective mentalizing	POFA, FPT, TECA self-rated	No	=	=	<	NA
Serra et al, 2016^Citation124	20 DM1 and 18 HC	Cognitive empathy and affective mentalizing	RMET, modified Happé	No	NA	<	<	NA

Abbreviations: BEES: Balanced Emotional Empathy Scale;¹³⁷ BES: Basic Empathy Scale;¹³⁸ EPT: Empathy for Pain Task;¹³⁹ EQ: Empathy Quotient Questionnaire;¹⁴⁰ FPT: Faux-Pas Test;¹⁴¹ GCPT: Guilford’s Cartoon Predictions Test;¹⁴² IRI: Interpersonal Reactivity Index;²⁰ MET: Multifaceted Empathy Test;¹⁴⁴ POFA: pictures of facial affect;¹⁴⁵ RMET: Reading the Mind in the Eyes Test;¹⁴⁶ SET: Story-based Empathy Task;⁵⁶ TASIT: The Awareness of Social Inference Test;¹⁴⁷ TECA: The Test of Cognitive and Affective Empathy.¹⁴⁸

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Data Availability

All data relevant to the study are included in the article.