assessing anosognosias after stroke: a review of the methods used and developed over the past 35...

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65666768697071727374
Review 7576777879808182
Assessing anosognosias after stroke: A review ofthe methods used and developed over the past 35years

83848586

Mari E. Nurmi (nee Laihosalo) and Mervi Jehkonen*

University of Tampere, School of Social Sciences and Humanities, Tampere, Finland
8788 8990919293949596979899
100101102103104105106

a r t i c l e i n f o

Article history:

Received 29 November 2013

Reviewed 11 January 2014

Revised 3 March 2014

Accepted 18 April 2014

Action editor Paul Jenkinson

Published online xxx

Keywords:

Anosognosia

Assessment

Awareness

Stroke

Unawareness

* Corresponding author. University of TampeE-mail address: [email protected] (M

107108109110111112113

Please cite this article in press as: Nurmi (the methods used and developed over th

http://dx.doi.org/10.1016/j.cortex.2014.04.0080010-9452/ª 2014 Elsevier Ltd. All rights rese

a b s t r a c t

This review provides an overview of research into anosognosia after stroke over the past 35

years. We are specifically interested in the assessment of anosognosia in group studies and

in how any changes in assessment procedures have impacted the study of anognosia. Our

work is based on a systematic review of reports drawn from electronic databases covering

the period from 1978 to 2013 (CINAHL, PubMedMEDLINE, PsycINFO, Web of Knowledge).

Sixty-four articles met the selection criteria. The results of our review show that a deeper

understanding has evolved of the multifaceted syndrome of anosognosia during the past

decade. The most recent studies made more extensive use of research, observational and

performance-based procedures as well as traditional interview methods. Modality speci-

ficities and patients with language impairment also receive closer consideration than

earlier. Furthermore, the results are more often obtained from homogeneous patient

groups. The limitations of recent anosognosia research include the diversity of assessment

methods used and the variation in the assessment times between and within patient

groups, and the tendency to rely on only 1 method to assess and diagnose anosognosia. In

order to improve the comparability of anosognosia studies it would be useful to have

guidelines for the number and type of assessment methods used in studying different

subtypes of anosognosia, and to focus on homogeneous patient samples. Furthermore, it is

recommended that more research be done to explore chronic anosognosia and its impact

on daily living.

ª 2014 Elsevier Ltd. All rights reserved.

114115
116 117118 119120121122123124
1. Introduction

The term anosognosiawas first introduced by Babinski in 1914

(quoted in Levine, Calvanio, & Rinn, 1991; Prigatano, 2010).

Anosognosia refers to the lack of awareness of motor, visual

re, School of Social Scien. Jehkonen).

nee Laihosalo), M. E., & Je past 35 years, Cortex

rved.

or cognitive impairment in patients with neurological dis-

eases (Prigatano, 2010). Recent research findings have shown

that anosognosia is a multifaceted syndrome with several

subtypes (e.g., for hemiplegia, cortical blindness or Anton’s

syndrome, visual field defect, memory loss or amnesia,

ces and Humanities, FIN-33014 University of Tampere, Finland.

125126127128129

ehkonen, M., Assessing anosognosias after stroke: A review of(2014), http://dx.doi.org/10.1016/j.cortex.2014.04.008

mailto:[email protected]

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http://dx.doi.org/10.1016/j.cortex.2014.04.008



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neglect and aphasia) (Prigatano, 2010). It can also co-exist with

alexithymia, denial, delusional symptoms such as anosodia-

phoria, misoplegia, personification, and kinaesthetic halluci-

nations (Antoniello, Kluger, Sahlein, & Heilman, 2010; Baier &

Karnath, 2008; Beis, Paysant, Bret, Le Chapelain, & Andre,

2007; Prigatano, 2009; Santos, Caeiro, Ferro, Albuquerque, &

Figueira, 2006; Spalletta, Ripa, Bria, Caltagirone, & Robinson,

2006; Zeller, Gross, Bartsch, Johansen-Berg, & Classen, 2011).

Anosognosia can occur regardless of generalized intellectual

impairment, confusion or diffuse brain damage (Bisiach &

Gemiani, 1991). It can manifest with various neurological

conditions such as stroke, traumatic brain injury, multiple

sclerosis, Parkinson’s disease, Huntington’s disease and Alz-

heimer’s disease (Prigatano, 2010). Our review focused pri-

marily on anosognosia following stroke. We use the term

anosognosia to describe unawareness of any defect or illness.

Anosognosia can appear for particular functions or for

illness in general, and the degree of anosognosia can vary

from mild to severe (Prigatano, 2010). It can manifest inde-

pendently at the verbal, explicit level and at the nonverbal,

implicit level (Berti, Ladavas, & Della Corte, 1996). Patients

may recover quickly within a few days or weeks after acute

brain injury, the conditionmay fluctuate over time, and itmay

persist for years or even remain permanent (Jehkonen,

Ahonen, Dastidar, Laippala, & Vilkki, 2000; Jehkonen,

Laihosalo, & Kettunen, 2006a; Marcel, Terner, & Nimmo-

Smith, 2004; Starkstein, Jorge, & Robinson, 2010).

There is no consensus on the cause of anosognosia, and

the multifaceted nature of the condition means it is probably

impossible to find any single comprehensive explanation.

There are several neuroanatomical and neuropsychological

explanations of what causes anosognosia, which have been

thoroughly reviewed among others by Baier and Karnath

(2008), Jenkinson, Preston, and Ellis (2011), Karnath, Baier,

and Nagele (2005), Orfei, Robinson, Bria, Caltagirone, and

Spalletta (2008), Orfei et al. (2007), and Starkstein et al.

(2010). However, these are not the focus of the current review.

Anosognosia is associated with lesions in the right hemi-

sphere (RH), specifically lesions in the dorsolateral portions of

frontal cortical areas, as well as with parieto-temporal and

right insula lesions (Berti et al., 2005; Orfei et al., 2008;

Starkstein et al., 2010). However, due to the difficulties in

assessing language impaired patients using methods that rely

on verbal abilities, the assessment of anosognosia in left

hemisphere (LH) patients may not be sensitive enough to

detect all anosognosic patients. In fact, it has been suggested

that anosognosia for motor deficits following LH damage is an

underestimated phenomenon (Cocchini, Beschin, & Della

Sala, 2012). The occurrence of anosognosia varies widely

depending on the assessment methods used, the patient

sample, assessment time and subtypes of anosognosia

(Jehkonen et al., 2006a).

The reason why anosognosia is assessed with such a di-

versity of methods is easy enough to understand: this is a very

complex, multifaceted and variable phenomenon. In order to

gain a full and proper understanding of anosognosia, it is

necessary to take account of both verbal and nonverbal forms

of anosognosia so that any dissociation between explicit and

implicit knowledge can be detected (Cocchini et al., 2012;

Orfei, Caltagirone, & Spalletta, 2009). The assessment should

Please cite this article in press as: Nurmi (nee Laihosalo), M. E., & Jthe methods used and developed over the past 35 years, Cortex

also include separate domain scores for different abilities or

functions in order to capture any modality specificities, and

also take into account the variation in the degree of anosog-

nosia, namely how mild or severe, partial or total the stage of

unawareness is (Cocchini et al., 2012; Jenkinson et al., 2011;

Orfei et al., 2009). As patients recover from anosognosia at

different rates, the time of assessment may also influence the

results on the occurrence of anosognosia (Cocchini et al., 2012;

Jenkinson et al., 2011; Orfei et al., 2009).

A number of reviews of anosognosia have been published

in recent years (e.g., Cocchini et al., 2012; Jenkinson et al., 2011;

Orfei et al., 2007, 2008). The present review focuses on original

group research articles from January 1978 to July 2013. We are

specifically interested in the assessment of anosognosia after

stroke in different stroke subgroups over the past 35 years and

in how any changes in assessment procedures have impacted

the study of anosognosia.

2. Materials and methods

2.1. Selection of articles

We applied the same method we have used in our earlier re-

views (Jehkonen et al., 2006a, 2006b) to identify the relevant

literature. First, we searched the Cochrane Library database in

order to seewhether therewere any recent or ongoing reviews

on this subject, but we found none. Then, we searched

CINAHL, PubMedMEDLINE, PsycINFO, and Web of Knowledge

for articles published between January 1978 and July 2013. Due

to the wide range of definitions and the different levels of

accuracy with which anosognosias are described, we used the

search terms “stroke and anosognosia”, “stroke and unawareness”,

and “stroke and awareness”. The following inclusion criteria

were applied: English articles, studies on human and adult

subjects (>18 years). Studies concentrating on symptoms

related to anosognosia such as alexithymia, denial, delusional

symptoms such as anosodiaphoria, misoplegia, personifica-

tion, and kinaesthetic hallucinations were excluded. We also

excluded studies that were only concerned with the effects of

a specific intervention method.

The search terms “stroke and anosognosia” yielded 517 ab-

stracts, of which 59 met the inclusion criteria. The terms

“stroke and awareness” produced 3292 abstracts, of which, 32

met the inclusion criteria; and the terms “stroke and un-

awareness” yielded 694 abstracts, of which, 29 met the inclu-

sion criteria. After the removal of duplicate abstracts, in total,

64 of the 4503 abstracts met our inclusion criteria. The deci-

sion on which studies to include in the review was made by 2

independent reviewers.

3. Results

3.1. Patient selection

The sample sizes and patient characteristics are described in

Table 1. The number of patients in the 64 studies included in

our review ranged from 8 to 1059 [average: 99, median (Md):

50]. Patients’ age ranged from 19 to 100 years (average: 65, Md:




T ble 1 e Characteristics of the 64 articles reviewed Q5.

uthors and year Year N Patient selection Side of lesion Mean age(range)

Mean time sincestroke (range)

Assessment tools Type ofanosognosia(prevalence %)

utting, 1978 1978 70 Acute hemiplegia RH þ LH þ bilateral 66 4 days Cutting’s

questionnaire

For hemiplegia (RH

58%, LH 14%)

ier et al., 1983a,

1983b

1983 41 Selected from

consecutively evaluated

patients, first-ever

stroke

RH 59 Within 7 days Classification by Hier Denial of illness

(36%)

ier et al., 1983a,

1983b

1983 41 Selected from

consecutively evaluated

patients, first-ever

stroke

RH 59 13.5 weeks Classification by Hier After 11 weeks 13%

had denial of illness

isiach et al., 1986 1986 97 Right-handed, 82

vascular, 15 neoplastic

RH 63 (34e84) 7 days (1e37) Bisiach’s scale For hemiparesis (33%

medium or severe),

for visual field defect

(88%)

otomura et al., 1988 1988 46 Consecutive stroke

inpatients

RH 67 (45e84) N/A Method described by

Mori (1982)

General (37%)

nderson & Tranel, 1989 1989 32 Right-handed stroke

patients

RH þ LH 58 (28e83) Within 3e25 days Interview by

Anderson and Tranel

(1989)

For hemiparesis

(28%, all RH), for

cognitive deficits

(72%)

ibbard, Gordon, Stein,

Grober, & Sliwinski, 1992

1992 82 Recruited from inpatient

and outpatient

rehabilitation programs

RH þ LH 67 (45e85) 50 weeks Awareness

Questionnaire by

Hibbard

Unawareness of

stroke occurrence

(mild RH 20% LH

20%, severe RH 4%

LH 2%), Minimized

awareness of leg

paralysis (RH 30% LH

12%), of arm

paralysis (RH 40%,

LH 18%), of language

loss (RH e LH 25%),

of change in

abstraction abilities

(RH 50% LH 54%), of

memory change (RH

19% LH 19%)

tarkstein et al., 1992 1992 80 First-ever stroke,

selected from

consecutive admissions

N/A 62 6 days Starkstein’s

questionnaire

General (34%, mild

30%, moderate 33%,

severe 37%)

(continued on next page)

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Table 1 e (continued )

Authors and year Year N Patient selection Side of lesion Mean age(range)



Starkstein et al., 1993 1993 16 Anosognosic and non-

anosognosic first-ever

stroke patients, selected

from 24 consecutive

admissions to hospital

N/A, patients matched

for lesion side

61 5.5 days Starkstein’s

questionnaire

General (an

inclusion criteria;

mild 12%, moderate

38%, severe 50%)

Stone, Halligan, &

Greenwood, 1993

1993 171 Consecutively admitted

emergencies, first-ever

stroke

RH þ LH 72 (28e100) (2e3 days) Cutting’s

questionnaire

Denial or lack of

awareness of a

hemiparesis (RH

28%, LH 5% in a

subgroup of 116

patients)

Blonder & Ranseen, 1994 1994 10 Recruited from hospital

admissions

RH 66 (45e77) 22 days (2e42) Modified PCRS For hemiplegia 0%,

for

neuropsychological

deficits 0%

Godefroy et al., 1994 1994 11 First-ever stroke RH þ LH 56 (18e79) Acute stage, 6-week

follow-up

(1) Shortened

evaluation of Anton

eBabinski

syndrome; (2)

Bisiach scale

The AntoneBabinski

syndrome: acute

(27%, all RH), follow-

up (0%)

Starkstein et al., 1994 1994 59 First-ever stroke,

selected from 65

consecutive admissions

to hospital

N/A 58 6 days Starkstein’s

questionnaire

General (27%)

Grotta & Bratina, 1995 1995 24 Selected group of

thrombolytic patients

RH þ LH þ N/A N/A (2 dayse14 months) Interview by Grotta

and Bratina

Poor awareness of

the type and severity

of their neurological

deficit (50%; RH 57%,

LH 33%),

unawareness of the

improvement in the

clinical condition

(75%)

Berti et al., 1996 1996 34 Selected in geriatric

department, chronic

patients with complete

left hemiplegia

RH 71 (55e87) 60 days (30e545) Berti’s procedure For motor

impairment (27%),

for neglect dyslexia

(60%), for drawing

neglect (47%)

Hjaltason, Tegner,

Tham, Levander,

& Ericson, 1996

1996 17 Chronic neglect patients

who had moderate or

severe neglect 1e5 years

before examination

RH 63 124 weeks Questionnaire by

Hjaltason

Unawareness of

disability (0%)

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Jorgensen et al., 1996 1996 1059 Unselected acute stroke

patients

N/A 74 On admission N/A General (25%)

Pedersen, Jorgensen,

et al., 1996

1996 566 Community-based

setting, all patients

included, 122 had prior

stroke

RH þ LH 74 On admission Bisiach’s scale General (21%, 36%

RH, 9% LH)

Pedersen, Wandel,

et al., 1996

1996 327 Community based,

includes all kind of

stroke patients

RH þ LH 76 On admission Bisiach’s scale General (40%, in a

subgroup of 205

patients)

Pedersen et al., 1997 1997 602 Acute stroke patients,

21% had previous stroke

RH þ LH 74 On admission Bisiach’s scale General (21%, in

patients with

hemineglect 73%,

without hemineglect

6%)

Ghika-Schmid

et al., 1999

1999 53 Consecutive patients,

first-ever stroke

RH þ LH þ bilateral 60 (0e7 days), 3-month

follow-up

Standardized

interview by Ghika-

Schmid

Complete verbal

denial of symptoms

(anosognosia) (15%;

RH 88%, LH 12%)

Jehkonen et al., 2000 2000 56 Consecutive patients,

first-ever stroke

RH 63 6 days (2e10), 3-

month and 12-

month follow-ups

(1) Direct question by

Jehkonen; (2)

Cutting’s

questionnaire

For neglect (acute

25%, 3-month 9%, 12-

month 7%), for

hemiparesis (acute

14%, 3-month 0),

unaware of illness

(acute 11%, 3-month

0)

Karussis et al., 2000 2000 16 Consecutive patients

with pure thalamic

stroke

RH þ LH 75 N/A Interview by Levine General (31%, all RH)

Hartman-Maeir

et al., 2001

2001 46 Selected sample, with

severe motor deficit,

first-ever stroke

RH þ LH 57 44 days (1) Ramachandran’s

procedure; (2)

Interview by

Anderson & Tranel

For hemiplegia (RH

28%, LH 24%)

Jehkonen et al., 2001 2001 49 Consecutive patients,

first-ever stroke

RH 63 6 days (2e10), 12-

month follow-up

(1) Direct question by

Jehkonen; (2)

Cutting’s

questionnaire

For hemiparesis

(14%), for neglect

(27%), unawareness

of illness (12%)

Appelros et al., 2002 2002 276 Population-based study

of all cases of first-ever

stroke

RH þ LH þ N/A 77 Within the first

month

Starkstein’s

questionnaire

General (17%)

Azouvi et al., 2002 2002 206 Consecutive first-ever

stroke

RH 56 11 weeks (1) Bisiach’s scale; (2)

CBS

For hemiplegia

(17%), for visual

impairments (46%),

for behavioural

neglect (37%)


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able 1 e (continued )

uthors and year Year N Patient selection Side of lesion Mean age(range)

Mean time sinstroke (range


artman-Maeir

et al., 2002

2002 60 Selected sample, first-

ever stroke, right-

handed, admitted to

rehabilitation hospital

RH þ LH 58 43 days, follow-u

347 days

Interview by

Anderson & Tranel

Total unawareness

of deficits: (mild 50%,

moderate 22%,

severe 2%),

unawareness of

deficit in motor: (RH

6%, LH 13%), visual

field: (RH 3%, LH 8%),

thinking: (RH 58%,

LH 67%), orientation-

time: (RH 11%, LH

21%), orientation-

place: (RH 6%, LH

29%), memory: (RH

25%, LH 21%), visual

attention: (RH 39%,

LH 21%), illness (RH

25%, LH 33%)

aguire & Ogden, 2002 2002 9 Patients with stroke and

persistent neglect

RH þ LH 55 (41e63) (3e22 months) Bisiach’s scale For visual field

unilateral neglect

(89%), for motor

deficit (78%), for

personal neglect

(100%).

isser-Keizer et al., 2002 2002 113 Consecutive first-ever

ischaemic stroke

RH þ LH 67 3 months, 15-mo

follow-up

Interview by Visser-

Keizer

General (N/A)

ppelros et al., 2003 2003 276 Population-based study


stroke

RH þ LH þ N/A 75 Within the first

month, a 1-year

follow-up for 7

survivors with

anosognosia

Starkstein’s

questionnaire

General, acute stage:

(17%), after 1 year

(0%)

artman-Maeir

et al., 2003

2003 60 Consecutive right-

handed patients

admitted to

rehabilitation hospital,

first-ever stroke

RH þ LH 57 43 days, follow-u

347 days

Discrepancy score

on FIM motor scale

by Hartman-Maeir

Overestimation of

ADL competency (at

admission RH 53%,

LH 42%; at discharge

RH 27%, LH 23%)

eis et al., 2004 2004 78 First-ever stroke,

consecutively included

LH 55 11 weeks Bisiach’s scale For hemiplegia (6%),

for visual

impairments (10%)

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Marcel et al., 2004 2004 64 Patients with

hemiplegia

RH þ LH 72 67 days (1) Interview by

Anderson and

Tranel; (2) procedure

by Marcel

Explicit, for motor

deficit (23%), for

visual field defect

(45%), for

somatosensory

deficit (80%),

implicit, for motor

deficit (in arm RH

31%, LH 0; in leg RH

26%, LH 0), for

sensation (in arm RH

61%, LH 19%: in leg

RH 39%, LH 6%), for

verbal fluency (RH

36%, LH 36%), for

working memory

(RH 19%, LH 29%)

Baier & Karnath, 2005 2005 128 Patients with

hemiparesis or

hemiplegia

RH þ LH Md 72 (20e100) Md 4 days (0e15) Bisiach’s scale For hemiplegia (23%,

RH 59%, LH 41%)

Gialanella et al., 2005 2005 30 Selected sample of

neglect and/or

anosognosic patients

with severe motor

impairment

RH 70 (N þ 68.2,

N þ Aþ 72.1)

23 days, follow-up:

59 days

Bisiach’s scale For hemiplegia (an

inclusion criteria), at

discharge all

anosognosic

patients had explicit

awareness, but

implicit

unawareness

Hochstenbach et al., 2005 2005 172 Home-based stroke

patients

RH þ LH þbilateral þ N/A

55 (18e70) 10 months Interview by

Hochtenbach

Agreement between

patients’ and

relatives’ complaints

(N/A)

Nimmo-Smith, Marcel, &

Tegner, 2005

2005 64 Patients with

hemiplegia

RH þ LH 72 67 days (1) Interview by

Anderson and

Tranel; (2) Marcels

bilateral task

questions

For motor deficit,

explicit (26% RH, 9%

LH), implicit (52% RH,

5% LH 0%)

Azouvi et al., 2006 2006 421 Patients recruited from

rehabilitation wards

RH þ LH 55 12 weeks (1) Bisiach’s scale; (2)

CBS

For hemiplegia (RH

17%, LH 6%), for

hemianopia (RH 46%,

LH 10%), for neglect

(RH 37%)

Appelros et al., 2007 2007 272 Population-based study


stroke

RH þ LH þ N/A 76 (1e4 days), 1-year

follow-up

Starkstein’s

questionnaire

General (17%)


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Ekstam et al., 2007 2007 26 Longitudinal

prospective study of

patients participating in

rehabilitation at home

RH þ LH þ N/A Md 82 (75e84) 1month, 3, 6, and 12-

month follow-ups

AAD Unawareness of

disability (N/A)

Spalletta et al., 2007 2007 50 Consecutive first-ever

stroke patients from


RH 67 41 days Bisiach’s scale For motor

impairment (26%)

Fotopoulou et al., 2008 2008 8 Consecutive acute

stroke unit patients with

first-ever stroke and

complete left upper limb

hemiplegia

RH 62 20 days (1) Berti’s procedure

(interview) (2)

Feinberg’s

Questionnaire (3)

Rubber hand

experiment

For hemiplegia (50%,

basis for division

into experimental

groups)

Langer & Samuels, 2008 2008 25 Consecutive first-ever

stroke patients from an

acute rehabilitation

ward

RH þ LH 63 12 days (1) Clinical

Awareness; (2)

Medical Awareness;

(3) PCRS

Unawareness of

disability (50%)

Cocchini et al., 2009 2009 33 Patients with motor

impairment

LH 70 (42e87) 74 days (7e210) (1) Berti’s procedure

(interview); (2)

VATAm

For motor

impairment (Berti:

10%; VATAm: 40%)

Gialanella et al., 2009 2009 33 First-ever CVA patients

with left hemiparesis,

anosognosia and/or

neglect recruited from


RH 69 42 days Bisiach’s scale For hemiplegia (an

inclusion criteria)

Della Sala et al., 2009 2009 63 Patients with unilateral

lesions from

rehabilitation ward

RH þ LH 70 (29e87) 62 days (4e210) VATAm Explicit, for motor

impairment (total

41%; RH 42%, LH 40%)

Jenkinson, Edelstyn,

Drakeford, et al., 2009

2009 17 Consecutive acute

stroke ward patients

with a dense left

hemiplegia

RH 68 14 days (1) Berti’s procedure;

(2) Reality

monitoring task


basis for division

into experimental

subgroups)


& Ellis, 2009

2009 18 Consecutive acute

stroke ward patients

with a dense left

hemiplegia

RH 65 8 days (1) Berti’s procedure;

(2) Grip selection

task


basis for division

into experimental

subgroups)

Scott et al., 2009 2009 67 Eligible patients

recruited prior to

discharge from

rehabilitation units

RH þ LH þ bilateral 58 52 months/Md 28

months

Ratings of driving

ability

Impaired self-

awareness (N/A)

Cocchini, Beschin, et al., 2010 2010 30 RH patients with upper

limb paresis

RH 66 (29e87) 56 days (13e149) (1) VATAm (2) BMT For motor

impairment (explicit

43%, implicit 23%)

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Cocchini, Gregg, et al., 2010 2010 53 Aphasic patients

recruited from


LH þ bilateral 57 (19e84) 300 days (6e3963) VATA-L For aphasia (19%)

Fotopoulou et al., 2010 2010 14 Consecutive acute

stroke unit patients with

first-ever stroke and

complete left upper limb

hemiplegia

RH 60 20 days (1) Berti’s procedure

(interview) (2)

Feinberg’s

Questionnaire (3)

Fotopoulou’s

implicit and explicit

tests


basis for division

into experimental

groups)

Ishii et al., 2010 2010 49 Consecutive series of

right-handed stroke

patients attending a

rehabilitation

programme

RH þ LH 69 16 days Bisiach’s scale General (67% in a

subgroup of 12

patients)

Vocat et al., 2010 2010 58 Prospectively screened

hospital patients with

first-ever stroke and left

arm motor impairment

RH 64 Hyperacute: 3 days (1

e5), subacute: 8 days

(7e12), chronic: 223

days (180e273)

(1) Bisiach’s scale; (2)

Modified

Anosognosia for

Hemiplegia

Questionnaire (3)

Marcel’s and Berti’s

Confrontation

procedure; (4)

Cutting’s

questionnaire; (5)

CBS; (6) Open

interview on

patients experience

of symptoms

Explicit, for

hemiplegia:

hyperacute: 50e44%;

subacute: 43e38%;

chronic: 11e5%;

Implicit, for motor

impairment:

hyperacute: 69%;

Subacute: 52%;

Chronic: 5%

McKay et al., 2011 2011 30 First-ever stroke

patients recruited at

discharge from different

stroke clinics

RH þ LH þ bilateral 54 (32e70) 46 months (3e280)/

Md 15 months

Metacognitive

pretest and posttest

discrepancy score

Impaired self-

awareness (N/A)

Moro et al., 2011 2011 24 First-ever stroke

patients with severe

hemiplegia and

anosognosia were

recruited from

rehabilitation unit

RH þ LH 64 (40e79) (1) Berti’s procedure

(interview); (2)

Marcel’s Interview;

(3) Interview about

the impairment in

non-motor

functions; (4)

Experimental tasks

for implicit and

emergent awareness

For motor

impairment (an

inclusion criteria:

implicit (58%),

emergent awareness

(25%)), for neglect

(6%), for memory

deficits (57%), for

temporal

disorientation (50%)

Garbarini et al., 2012 2012 10 Right-handed first-ever

stroke patients with

hemiplegia and

anosognosia or neglect

RH Md 71 (66e84) Md 32 days (25e65) (1) Berti’s procedure;

(2) VATAm; (3)

Circleselines

bimanual motor task

For hemiplegia (an

inclusion criteria)


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Mattioli, Gialanella,

Stampatori, & Scarpazza,

2012

2012 38 Consecutive first-ever

stroke patients

RH 69 41 days Bisiach’s scale For hemiplegia (34%)

Vossel et al., 2012 2012 56 Patients with unilateral

RH stroke

RH 60 112 days 1) Index for the

degree of

unawareness for

visuospatial neglect;

(2) Sharer’s

Questionnaire

For visuospatial

neglect (N/A, basis

for division into

subgroups)

Cocchini et al., 2013 2013 30 Patients recruited from


LH þ bilateral 61 (19e84) 41 weeks (1e306) (1) VATAm; (2)

VATA-L

For motor

impairment (46%),

for language

impairment (24%)

Kottorp et al., 2013 2013 183 Data records from

Assessment of

Awareness of Ability

database

RH þ LH 66 N/A AAD Unawareness of

disability (N/A)

Vocat et al., 2013 2013 9 Consecutive first-ever

stroke patients with a

full left hemiplegia

RH 58 11 days (1) Bisiach’s scale (2)

Riddle test

For hemiplegia (44%)

Vossel et al., 2013 2013 55 Consecutively recruited

hospital patients

RH 59 115 days (1) Index for the

degree of

unawareness for

visuospatial neglect;

(2) Sharer’s

Questionnaire

For hemiparesis

(18%); anosognosia

for visuospatial

deficit (N/A)

Abbreviations: AAD ¼ Assessment of Awareness of Disability; BMT¼ Behavioural Motor Task; CBS¼ Catherine Bergego Scale; PCRS ¼ Patient Competency Rating Scale; VATA-L¼ Visual-Analogue Test

for Anosognosia for Language Impairment; N/A ¼ not available Q6Q7.

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c o r t e x x x x ( 2 0 1 4 ) 1e2 1 11

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64). Twenty-six (41%) of the 64 studies used consecutive series

of patients, 15 (23%) studies used motor impairment as an

inclusion criterion, 7 (11%) studies used anosognosia and/or

neglect as an inclusion criterion, 1 study recruited patients

with pure thalamic stroke, 1 study recruited patients with

lenticulostriate infarcts, and 1 study used language impair-

ment as an inclusion criteria. Twenty-four (38%) studies

recruited only RH patients and 4 (6%) studies recruited only

LH patients or patients with LH and bilateral damage. Twenty-

two (34%) studies had both RH and LH patients, 10 (16%)

studies had patients with RH and LH and/or bilateral damage

and/or patients whose lesion laterality was not classified (N/

A). Four (6%) studies did not specify lesion site. Six studies

were published during the time period from 1978 to 1989, 19

studies between years 1990 and 2001, and 39 studies between

years 2002 and 2013.
8384858687888990919293949596979899
100101102103104105

3.2. Assessment methods and timing

3.2.1. Assessment of anosognosiasTable 2 describes the methods used to assess anosognosia,

and Table 3 summarizes the most frequently used methods

during different periods. All told, the studies reviewed used 41

different methods. From 1978 to 1989 6 new assessment

methods were developed, all concentrating on the evaluation

of explicit anosognosia, and 1 method used a discrepancy

score. From 1990 to 2001 the number of new methods intro-

duced was 14, 12 of which evaluated explicit anosognosia, 1

evaluated implicit anosognosia and 1 both explicit and im-

plicit anosognosia. Five of these methods used discrepancy

scores. From 2002 to 2013 the number of new methods intro-

duced was 21, 12 of which evaluated explicit anosognosia, 7

evaluated implicit anosognosia, and 2 methods evaluated

both explicit and implicit anosognosia. Six of these methods

used discrepancy scores, and 7 methods were experimental

designs.

Table 2 e Description of the assessment methods for anosogno

Assessment methods Scaling

Cutting’s questionnaire

(1978)

Dichotomous classification

(having/not having anosognosia)

Clin

Method described by Mori

(1982)

Unknown (original article in

Japanese)

Hier et al. (1983a, 1983b) Dichotomous classification

(patients who fail to acknowledge

either deficits or stroke are rated as

anosognosic)

Clin

Anosognosia scale by

Bisiach et al. (1986)

4-point scale: 0 ¼ no anosognosia,

1 ¼ mild, 2 ¼ moderate, and

3 ¼ severe

Clin

PCRS by Prigatano et al.

(1986)

5-point Likert scale from 1

(¼patient cannot perform the

activity) to 5 (¼patient can perform

the activity with ease);

anosognosia is defined by the

degree of discrepancy between the

patient and clinician/caregiver

score

Self-

care

Clin


From 1978 to 1989 all the studies reviewed used only 1

assessment method to define the presence of anosognosia.

From 1990 to 2001 73% of the studies used only 1 assessment

method, 22% used 2 methods, and 1 study did not describe

how anosognosia was assessed. From 2002 to 2013 54% of the

studies used only 1 method to assess anosognosia, 31% used 2

methods, and 10% used 3 assessment methods. Furthermore,

1 study used 4 assessment methods, and 1 study used 6

assessment methods to study anosognosia.

3.2.2. Timing of the first evaluation and follow-up studiesTable 1 reports the assessment times as given in the 64 articles

reviewed. The timing of the assessment varied widely in the

articles reviewed, and patient samples in the same studies

could include patients at the acute, subacute and chronic

stage of stroke. Two studies (Cocchini, Beschin, Cameron,

Fotopoulou, & Della Sala, 2009; Vossel, Weiss, Eschenbeck, &

Fink, 2013) acknowledged this and divided their patients into

subgroups according to the time of stroke onset. In 1978e1989

the timing of the first assessment ranged from less than a

week to 13.5 weeks, in 1990e2001 from 1 day to 124weeks, and

in 2002e2013 from 0 days to 1120weeks. Seven articles did not

report their exact assessment times (Godefroy, Rousseaux,

Pruvo, Cabaret, & Leys, 1994; Jorgensen, Nakayama, Reith,

Raaschou, & Olsen, 1996; Karussis, Leker, & Abramsky, 2000;

Kottorp, Ekstam, & Petersson, 2013; Motomura, Sawada,

Inoue, Asaba, & Sakai, 1988; Pedersen, Jorgensen, Nakayama,

Raachou, & Olsen, 1996, 1997; Pedersen, Wandel, et al., 1996).

The majority of the articles had no follow-up. Twelve (19%)

studies (Appelros, Karlsson, & Hennerdal, 2007; Appelros,

Karlsson, Seiger, & Nydevik, 2003; Ekstam, Uppgard, Kottorp,

& Tham, 2007; Ghika-Schmid, van Melle, Guex, & Bogous-

slavsky, 1999; Gialanella, Monguzzi, Santoro, & Rocchi, 2005;

Godefroy et al., 1994; Hartman-Maeir, Soroker, Oman, & Katz,

2003; Hartman-Maeir, Soroker, Ring, & Katz, 2002; Jehkonen

et al., 2000, 2001; Visser-Keizer, Jong, Deelman, Berg, &

sia according to publishing date.

Administration Forms of anosognosiaassessed

ician-rated scale Explicit anosognosia for motor

deficits

ician-rated scale Explicit anosognosia for illness

ician-rated scale Explicit anosognosia for

sensorimotor impairment or visual

field defect

rated scale and clinician/

giver-rated scale

Explicit anosognosia for cognitive

deficits

ician-rated scale


106107108109110111112113114115116117118119120121122123124125126127128129130





Assessment methods Scaling Administration Forms of anosognosiaassessed

Awareness Interview by

Anderson and Tranel

(1989)

3-point scale: 1 ¼ patient

acknowledges problems,

2 ¼ patient describes mild

problems, 3 ¼ patient denies any

problems

Unawareness of cognitive

impairments and motor defects in

patients with brain damage caused

by cerebral infarction, dementia, or

head trauma

Interview by Levine et al.

(1991)

Not specified Clinician-rated scale Explicit anosognosia for motor

deficits

Anosognosia Questionnaire

by Starkstein et al. (1992)

4-point scale: 1 ¼ no anosognosia,

2 ¼ mild, 3 ¼ moderate, 4 ¼ severe

Clinician-rated scale Explicit anosognosia for motor and

visual deficits

Awareness Questionnaire

by Hibbard et al. (1992)

3-point classification: 1 ¼ patients’

self-report accurate when

compared to the objective data,

2 ¼ patients’ self-report

minimized, 3 ¼ patients’ self-

report exaggerated

Self-rated scale Explicit unawareness of physical,

cognitive, and affective changes

poststroke

Shortened evaluation of

AntoneBabinski

syndrome used by

Godefroy et al. (1994)

Not specified Not specified Anosognosia for blindness

Task choice method by

Ramachandran (1995)


(patients who attempt and fail to

perform 1 or 2 bimanual tasks are

rated as anosognosic)

Clinician-rated scale Implicit anosognosia for

hemiplegia

Interview by Grotta and

Bratina (1995)

Not reported Clinician-rated scale Explicit awareness of the type,

severity and improvement of

neurological deficit

Assessment procedure by

Berti et al. (1996)

3-point scale: 0 ¼ normal, 1 ¼ mild

anosognosia, 2 ¼ severe

anosognosia; 10-point scale from

0 (¼perform very badly) to 10

(¼perform very well)

Clinician-rated scale, self-rated

scale

Explicit and implicit anosognosia

for hemiparesis and unawareness

of higher-order cognitive defects

related to neglect

Awareness of disability

questionnaire for patients

and relatives by Hjaltason

et al. (1996)

5-point scale: 1¼ cannot do it at all,

2 ¼ very difficult, 3 ¼ some

difficulty, 4 ¼ fairly easy, 5 ¼ very

easy; awareness is defined by the



score

Self-rated scale and clinician/

caregiver-rated scale

Explicit awareness of disability

CBS by Azouvi et al. (1996) 4-point scale: 0 ¼ no difficulty,

1 ¼ mild difficulty, 2 ¼ moderate

difficulty, 3 ¼ severe difficulty;

anosognosia is defined by the



score



Explicit anosognosia for neglect

Awareness Questionnaire

by Sherer, Bergloff, Boake,

High, and Levin (1998)

5-point Likert scale: 1 ¼ none,

2 ¼ minimal, 3 ¼ moderate,

4 ¼ severe, or 5 ¼ complete lack of

awareness of deficits; awareness is

defined by the degree of

discrepancy between the patient

and clinician/caregiver score



Explicit impaired self-awareness

AAD by Tham, Bernspang,

and Fisher (1999)

4-point scale from 1 (major) to 4 (no

discrepancy)

Clinician-rated scale Explicit anosognosia for disability

Standardized interview

about the patients acute

appreciation of their

condition by Ghika-

Schmid (1999)

Not reported Clinician-rated scale Explicit anosognosia

Anosognosia for Hemiplegia

Questionnaire by

Feinberg et al. (2000)

3-point scale: 0 ¼ full awareness,

.5 ¼ partial awareness,

1 ¼ complete unawareness

Clinician-rated scale Explicit anosognosia for motor

deficits

Direct question by

Jehkonen et al. (2000)


(having/not having anosognosia)

Clinician-rated scale Explicit anosognosia for neglect

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Please cite this article in press as: Nurmi (nee Laihosalo), M. E., & Jehkonen, M., Assessing anosognosias after stroke: A review ofthe methods used and developed over the past 35 years, Cortex (2014), http://dx.doi.org/10.1016/j.cortex.2014.04.008





Interview for patients and

partners by Visser-Keizer

et al. (2002)

4-point scale from 0 (¼not

changed) to 3 (¼very much

changed); discrepancy is measured

by subtracting partner scores from

patient scores

Self-rated scale, caregiver-rated

scale

Explicit anosognosia for emotional

and cognitive changes

Discrepancy score on FIM

motor scale by Hartman-

Maeir et al. (2003)

Discrepancy between therapist and

patient rating was the measure for

unawareness. A difference of 5

points or more in the total score or

2 points or more in the item scores

were used as the criteria for

underestimation or overestimation

of abilities


scale

Explicit unawareness of disabilities

in basic ADL

Structured Awareness

Interview by Marcel et al.

(2004)

(1) Interview: 3-point scale

(‘Aware’, ‘Unaware’,

‘Inapplicable’); (2) Performance

rating: 1 ¼ patient’s evaluation

correct, 2 ¼ minor overestimation,

3 ¼ major overestimation


scale


for motor impairment

Semistructured interview to

patients and relatives by

Hochstenbach et al. (2005)

Dichotomous classification:

0 ¼ complaint absent or

1 ¼ complaint present; the

agreement score between patients

and relatives was calculated


scale

Explicit anosognosia

Clinical Awareness by

Langer and Samuels

(2008)

7-point scale, from no impairment

(¼7) through severe impairment

(¼1)

Clinician-rated scale Explicit anosognosia for illness

Medical Awareness by

Langer and Samuels

(2008)

4-point Likert scale: 0 ¼ severe,

1 ¼ moderate, 2 ¼ mild, 3 ¼ none

Clinician-rated scale Explicit anosognosia for illness

Rubber hand experiment by

Fotopoulou et al. (2008)

(1) Movement detection score: ‘Did

your left hand move?’ (YES/NO

response); (2) Measures confidence

rating: Likert-type scale from 1 to 7;

(3) Agency scores over the observed

movement: ‘Did you or someone

else move your hand?’ (‘Me/

Someone else’ response)

Self-rated scale Implicit awareness of motor

function

Grip selection task by

Jenkinson, Edelstyn, and

Ellis (2009)

The motor imagery accuracy was

calculated with a formula taking

into account the orientation of the

stimulus, hand used (left/right),

imagery hand positions reported

by patient and the actual hand

position when grasping the handle

Clinician-rated scale Implicit motor awareness

Ratings of driving ability for

patients and partners by

Scott et al. (2009)

5-point scale ranging from 1

(¼poor) to 5 (¼excellent); patients

and caregivers rated their own and

companions’ driving ability

compared to the average driver and

compared to their survey

companion


scale

Explicit awareness for disability

Reality monitoring task by


Drakeford, et al. (2009)

A studiedeunstudied judgement:

hit/false. The reality monitoring

data are reported as source

proportion (¼the number of items

assigned to a correct source

divided by the total number of hits)

Clinician-rated scale Impaired reality monitoring in

anosognosia

VATAm by Della Sala et al.

(2009)

4-point visual-analogue scale from

0 (¼no problem) to 3 (¼severe

problem); anosognosia is defined

by the degree of discrepancy


scale

Explicit anosognosia for motor

deficits, suitable for aphasic

patients


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between the patient and caregiver

score

Assessment of subjective

experience of symptoms

by patients’ verbal report

by Vocat et al. (2010)

3-point scale: 0 for full, 1 for

incomplete and 2 for absent report

of the expected correct experience

An open interview Explicit impaired self-awareness

BMT by Cocchini, Beschin,

et al. (2010)

4-point scale: 0 ¼ patient promptly

carries out the task using 1 hand,

1 ¼ patient carries out the task

using 1 hand but with some

hesitation, 2 ¼ patient started the

task as if they could use 2 hands

but then they corrected

themselves, 3 ¼ patient behaved as

if he/she could use 2 hands

resulting in a failure due to

anosognosia

Clinician-rated scale Implicit anosognosia for motor

awareness

Implicit and explicit tests

for anosognosia by

Fotopoulou et al. (2010)

(1) Implicit test: reaction times in

completing the sentences; (2)

Explicit test: scale from 1 (¼not

related) to 10 (¼extremely related

to my current situation)


scale


for motor impairment

Visual-Analogue Test for

Anosognosia for

Language Impairment by

Cocchini, Beschin, et al.

(2010) and Cocchini,

Gregg, et al. (2010)

4-point visual-analogue scale from

0 (¼no problem) to 3 (¼major

problem); anosognosia is defined

by the degree of discrepancy

between the patient and caregiver

score


scale

Explicit anosognosia for language

impairment, suitable for aphasic

patients

Experimental tasks for

implicit and emergent

awareness by Moro et al.

(2011)

(1) Implicit awareness: cut-off: 25%

of the length of the object patient is

holding in his hand (0 ¼ extreme

right, 50% centre, 100% extreme

left). Shift towards the midpoint

indexed implicit awareness; (2)

Emergent awareness: 4-point scale

(3 ¼ correct judgement before the

request to perform the action,

2 ¼ correct judgement when

subjects were about to start the

action, 1 ¼ subjects became aware

of their deficits after failure of the

action, 0 ¼ awareness of paralysis

did not improve after the failed

attempt to execute the action. A

mean score over the third quartile

was considered an index of

emergent awareness

Clinician-rated scale Implicit and emergent awareness

of motor function

Interview of Awareness of

impairment in non-motor

functions by Moro et al.

(2011)

Not specified Not specified Explicit anosognosia for non-motor

functions

Metacognitive pretest and

posttest discrepancy

score by McKay et al.

(2011)

Rating scale not specified;

Response options range frommuch

worse to much better than same-

age healthy peers

Self-rated scale Explicit impaired self-awareness of

ability

Circleselines bimanual

motor task by Garbarini

et al. (2012)

(1) Recorded movement

trajectories in bimanual tasks; (2)

5-point Likert scale: 0 ¼ absent,

1 ¼ poor, 2 ¼ medium, 3 ¼ good,

4 ¼ very good; Patients’ and

examiners’ evaluations of the

patients’ bimanual performance

are compared to produce a


scale

Implicit anosognosia for motor

awareness

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deviation score of motor

awareness

Index for the degree of

unawareness for

visuospatial neglect by

Vossel et al. (2012)

5-point scale ranging from 1

(¼severe difficulties) to 5 (¼no

difficulties); anosognosia index is

calculated by subtracting patient’s

self-rating from clinician’s rating

and divided by clinician’s rating


scale

Explicit anosognosia for

visuospatial neglect

Riddle test by Vocat et al.

(2013)

(1) Self-rated level of confidence: a

vertical visually presented scale

ranging from 0 (¼completely

unsure) to 8 (¼completely sure); (2)

Response type evaluated by

clinician: “correct response”, “false

response”, “repetition” or “no

response”; (3) A global score of

correct reasoning (scale not given)


scale

Deficits in cognitive monitoring

mechanisms

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Gerritsen, 2002; Vocat, Staub, Stroppini, & Vuilleumier, 2010)

conducted a follow-up between 6 weeks and 15 months, 2

studies (Jehkonen et al., 2000; Vocat et al., 2010) had 2 follow-

ups, and 1 (Ekstam et al., 2007) had 3 follow-ups.

3.3. Prevalence and subtypes of anosognosias

Table 4 provides a summary of the different subtypes of

anosognosia and their prevalence in patient subgroups ac-

cording to lesion side. Six (9%) studies did not report the

prevalence of anosognosia (Ekstam et al., 2007; Hochstenbach,

Prigatano, & Mulder, 2005; Kottorp et al., 2013; McKay,

Table 3 e Use of the most common anosognosiaassessment methods in different time periods.

Methods for assessinganosognosias

No. of studiesusing this methoda

1978e1989

Rating Scale by Bisiach et al. (1986) 1

Anosognosia Questionnaire by

Cutting (1978)

1

Awareness Interview by Anderson

and Tranel (1989)

1

1990e2001



Starkstein et al. (1992)

3


Cutting (1978)

2

Direct question by Jehkonen et al.

(2000)

2

2002e2013


Assessment procedure by Berti

et al. (1996)

8

VATAm by Della Sala et al. (2009) 5

Structured Awareness Interview by

Marcel et al. (2004)

4

a Note: Several studies used more than 1 measure.

102103104105106107108109110111112113114115116117


Rapport, Bryer, & Casey, 2011; Scott et al., 2009; Visser-Keizer

et al., 2002) and 5 (19%) studies (Fotopoulou, Pernigo, Maeda,

Rudd, & Kopelman, 2010; Fotopoulou et al., 2008; Jenkinson,

Edelstyn, Drakeford, & Ellis, 2009; Jenkinson, Edelstyn, &

Ellis, 2009; Vossel et al., 2012) used the presence of anosog-

nosia as a criterion for dividing patients into subgroups. Nine

(14%) studies (Appelros, Karlsson, Seiger, & Nydevik, 2002;

Baier & Karnath, 2005; Garbarini et al., 2012; Gialanella,

Mattioli, Rocchi, & Ferlucci, 2009; Gialanella et al., 2005;

Hartman-Maeir et al., 2002; Maguire & Ogden, 2002; Moro,

Pernigo, Zapparoli, Cordioli, & Aglioti, 2011; Starkstein,

Fedoroff, Price, Leiguarda, & Robinson, 1993) used anosog-

nosia as an inclusion criterion. These studies are excluded

from Table 4.

The prevalence of anosognosia varied according to the

assessment method used. For example, Vocat et al. (2010) re-

ported that the prevalence of explicit anosognosia for motor

impairment was higher when assessed with the scale devel-

oped by Bisiach, Vallar, Perani, Papagano, and Berti (1986) as

compared to assessments based on the Anosognosia for

Hemiplegia Questionnaire by Feinberg, Roane, and Ali (2000).

Della Sala, Cocchini, Beschin, and Cameron (2009) found that

the prevalence of anosognosia for motor impairment ranged

from 10% when assessed with the assessment procedure of

Berti et al. (1996) to 40% when assessed with the Visual-

Analogue Test for Anosognosia for Motor impairment

(VATAm) by Della Sala et al. (2009).
118119120121122123124125126127128129130
4. Discussion

In this review we have provided an overview of anosognosia

research over the past 35 years. Our main concern was with

the assessment of anosognosia after stroke and in how any

changes in assessment procedures have impacted the study of

anosognosia.

A growing interest to gain a deeper understanding of

anosognosia, its subtypes and the co-existing disorders is

seen in the anosognosia research during the past decade.




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There still remain many challenges with regard to the

comparability of results from different studies. The early

observation by McGlynn and Schacter (1989) regarding the

lack of conceptual clarity about the term anosognosia has

recently been reiterated by number of researchers (Jehkonen

et al., 2006a; Jenkinson et al., 2011; Orfei et al., 2008, 2007),

and this was clearly evident in our review as well. The ter-

minology concerning anosognosia is still rather confusing,

and descriptions of the different subtypes of anosognosia,

such as implicit versus explicit, verbal versus nonverbal,

behavioural, intellectual, emergent and anticipatory, also vary

widely. Unawareness, anosognosia and denial, for example,

are sometimes used interchangeably, at other times they have

differentmeanings in different studies. In some earlier studies

anosognosia and denial were used synonymously, but this

was not the case in more recent studies. This is positive

progress since anosognosia and denial are indeed different

symptoms that are caused by different mechanisms, and they

may have a differential impact on rehabilitation (Prigatano,

1996). Prigatano (1996) describes anosognosia as a negative

symptom in which impaired self-awareness represents a true

lack of information about impairments after brain injury.

Denial, then according to Prigatano (1996), is a positive

symptom that reflects patients’ attempts to cope with a

partially recognized problem. Anosognosic patients are typi-

cally unconcerned about failure and the negative feedback

about their behavioural or functional limitations, whereas

patients with denial will typically be angry or hostile and

demonstrate resistance when given negative feedback

(Prigatano, 1996). However, Prigatano and Klonoff (1998) point

out that patients can also show mixed symptoms and cannot

be classified as having only anosognosia or denial. Although it

can be difficult to make clear-cut distinctions between ano-

sognosia and symptoms related to anosognosia (e.g., denial,

anosodiaphoria, non-belonging, misoplegia), detailed and

elaborate definitions of these symptoms and the use of

objective methods are certainly useful to this end. Prigatano

and Klonoff (1998), for example, have developed a rating scale

for the brain-injured population to differentiate anosognosia

from denial.

In the recent anosognosia research there is a growing trend

to use more exact definitions of anosognosia. In previous de-

cades authors more often used the general term anosognosia

in their articles rather than making more specified definition

of which type of anosognosia they were referring to (13% of

the studies published in 2002e2013). In recent research au-

thors tend to define anosognosia according to its subtype (42%

of the studies published in 1990e2001).

During the past decade a key area of focus in anosognosia

research and in the development of new assessment methods

has been on anosognosia for motor impairment. This is un-

derstandable in view of the fact that hemiparesis is the most

easily observable deficit. Other subtypes of anosognosias have

also been assessed, such as anosognosia for neglect, for lan-

guage impairment, and for visual defect, but these need to be

explored in greater depth in order to gain a more compre-

hensive understanding of the syndrome of anosognosia after

stroke.

This lack of conceptual clarity and methodological con-

sistency is also reflected in the diversity of methods used to


assess anosognosia. The 64 studies reviewed used 41 different

methods for the assessment of anosognosia. The number of

measures available has increased sharply over the past

decade. Compared to the period from 1978 to 1989when 6 new

assessment methods were developed, the number of new

methods introduced from 2002 to 2013 was 21. A major focus

in recent years has been to develop more objective methods

for the assessment of anosognosia.

Based on the assessment methods used, recent research

into anosognosia has focused primarily on verbal, i.e., explicit

forms of anosognosia. However, implicit forms of anosognosia

have also attracted growing interest especially during the past

decade. Explicit, verbal anosognosia has been assessed using

structured questions addressed to the patient about their

deficits, and the information collected has then been

compared to different sources of information about the pa-

tient’s condition depending on the assessment procedure

used, for example medical records, neuropsychological per-

formance, or clinician’s evaluation (e.g., Berti et al., 1996).

Implicit forms of anosognosias have been evaluated by asking

patients to perform unimanual and/or bimanual tasks (e.g.,

Cocchini, Beschin, Fotopoulou, & Della Sala, 2010), or by

means of experimental designs (Fotopoulou et al., 2008, 2010;

Jenkinson, Edelstyn, & Ellis, 2009). Some procedures have been

modality-specific, using separate items for different deficits,

such as paresis of the upper and lower limbs (e.g., scale by

Bisiach et al., 1986; Structured Awareness Interview by Marcel

et al., 2004; Patient Competency Rating Scale by Prigatano

et al., 1986).

The most recent methods developed for the assessment of

anosognosias have also been used to test patients with lan-

guage impairment (Cocchini, Gregg, Beschin, Dean, & Della

Sala, 2010; Della Sala et al., 2009). These tools are the

VATAm (Della Sala et al., 2009), which was used in 5 studies

(Cocchini et al., 2009; Cocchini, Beschin, et al., 2010; Cocchini,

Crosta, Allen, Zaro, & Beschin, 2013; Della Sala et al., 2009;

Garbarini et al., 2012), and the Visual-Analogue Test assess-

ing Anosognosia for Language impairment (VATA-L; Cocchini,

Beschin, et al., 2010; Cocchini, Gregg, et al., 2010), which was

used in 2 studies (Cocchini et al., 2013; Cocchini, Gregg, et al.,

2010). When compared to more conventional methods, these

new methods allow for the assessment of a larger number of

language impaired patients. They have also helped to increase

the sensitivity of anosognosia diagnosis in LH stroke patients.

For example, traditional methods indicated that anosognosia

for hemiplegia occurred in 10% of all patients (as assessed

with Berti’s procedure), whereas the assessment procedure

designed for language impaired patients showed that it

occurred in 40% of the same patients (as assessed with

VATAm).

Experimental assessment procedures help to shed addi-

tional light on the syndrome of anosognosia and thereby

contribute to a more holistic understanding. Since experi-

mental procedures reviewed in this article concentrated

mainly on assessing anosognosia for motor impairment in RH

stroke patients, the results of these experimental procedures

have implications especially for the clinical assessment and

treatment of anosognosia for motor impairment. Experi-

mental studies (Fotopoulou et al., 2010; Moro et al., 2011) have

shown evidence of a dissociation between explicit and




Table 4 e Different subtypes of anosognosia and their prevalence according to lesion laterality in different time periods Q8.

Subtypes of anosognosia Prevalence %

RH LH/LH þ bilateral RH þ LH RH þ LH þ N/A/bilateral Not specified

1978e1989 (No of studies) n ¼ 4 n ¼ 0 n ¼ 1 n ¼ 1 n ¼ 0

For motor impairment (3) 33 e 28 14e58 e

For visual impairment (1) 88 e e e e

For cognitive impairment (1) e e 72 e e

For illness (1) 36 e e e e

General (1) 37 e e e e

1990e2001 n ¼ 5 n ¼ 0 n ¼ 8 n ¼ 2 n ¼ 4

For motor impairment (7) 14e27 e e 5e40 e

For visual impairment (1) e e 27 e e

For cognitive impairment (2) 0 e 19e54 e e

For language impairment (1) e e 25 e e

For neglect (3) 25e60 e e e e

For disability (3) 0 e e 15e50 e

For illness (3) 11e12 e 20 e e

For improvement (1) e e e 75 e

General (7) e e 21e40 e 25e34

2002e2013 n ¼ 15 n ¼ 4 n ¼ 13 n ¼ 7 n ¼ 0

For motor impairment (17) 17e69 6e46 5e78 e e

For visual impairment (5) 46 10 3e46 e e

For cognitive impairment (3) e e 6e67 e e

For language impairment (0) e e e e e

For neglect (4) 37 e 6e100 e e

For somatosensory deficit (1) e e 6e80 e e

For disability (2) e e 42e53 e e

For illness (1) e e 25e33 e e

General (6) e 19e24 67 17 e

Abbreviation: N/A ¼ lesion laterality not available.

Note: This table includes the 51 studies eligible. Note: Several studies addressed more than 1 subtype.

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implicit processing in anosognosia for motor impairment,

which lends support to the use of methods that can detect

both explicit and implicit forms of anosognosia. This will

provide a more in-depth picture of the patient’s condition,

which in turn is necessary for effective treatment and reha-

bilitation of anosognosia. The use of before/after procedures

in which patients perform actions and judge their actions is

useful in that they evaluate both explicit and implicit forms of

anosognosia. For example, a patient with hemiparesis of the

upper limb can claim that he or she is able to hold a traywith 2

hands, but in the execution of this task it may transpire that

the patient is in fact using only one hand, indicating implicit

knowledge of hemiparesis but not explicit awareness of the

condition. The use of confrontation is also recommended

since this method can shed light on the anosognosic patient’s

emergent awareness, i.e., possible changes in the patient’s

judgement of their ability to perform actions before and after

the execution of those actions. Moro et al. (2011) found that

the intention to act and/or actually acting may increase

explicit verbal knowledge of the deficit in some patients with

anosognosia for motor impairment when combined with

confrontation of the failure to act. There is also evidence that

chronic stroke patients examined after discharge from a

rehabilitation unit, who greatly overestimated their abilities in

familiar (driving) and in novel (neuropsychological) tasks,

benefit from immediate feedback upon task completion, and

their predictions becamemore accurate (McKay et al., 2011). In


addition, results from other recent experimental studies

(Fotopoulou et al., 2008; Garbarini et al., 2012; Jenkinson,

Edelstyn, Drakeford, et al., 2009; Jenkinson, Edelstyn, & Ellis,

2009) support the idea that motor awareness depends on a

comparison of the predicted and actual sensory consequences

of movement.

The involvement of impairment in higher-level monitoring

processes in anosognosia for hemiparesis has also been

explored. According to Vocat, Saj, and Vuilleumier (2013),

these high-level deficits can be observed not only in specific

functions related to motor actions or attention, but also in

other domains when patients are confronted with partial and

uncertain information. Patients with deficits in cognitive

monitoringmechanismsmay be abnormally confident in their

beliefs. They are also unable to change their beliefs evenwhen

confronted with new information that shows their views are

incongruent (Vocat et al., 2013). It is important that this

reduced ability to check and change current beliefs about

one’s own state despite the presence of incongruent infor-

mation is taken into account in the care and rehabilitation of

anosognosic patients. The use of imagery rehearsal training

combined with confrontation to failure to act as a rehabilita-

tion method may also be beneficial for at least some RH pa-

tients with anosognosia for motor impairment. There is

evidence that at least some anosognosic patients are able to

generate sufficient motor intentions/plans for the affected

hand, which is a key condition for imagery training in patients




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with anosognosia for hemiplegia (Garbarini et al., 2012).

However, as it seems that this is not the case with all ano-

sognosic patients (Jenkinson, Edelstyn, & Ellis, 2009), it is

recommended that the hemiplegic patient’s ability to form

motor representations is evaluated with a view to screening

those patients who would benefit from imagery rehearsal

(Jenkinson, Edelstyn, & Ellis, 2009).

Earlier reviews (Jehkonen et al., 2006a; Jenkinson et al.,

2011; Orfei et al., 2007, 2009; Starkstein et al., 2010) have

drawn attention to variation in the prevalence of anosognosia

and its possible causes (differences in patient selection,

assessment methods, subtypes assessed, diagnostic criteria,

assessment times, and lesion laterality).We found evidence of

this variation in the present review, too. In 1978e1989 the

prevalence of anosognosia ranged from 14% to 88%, in

1990e2001 from 0% to 60%, and in 2002e2013 from 3% to 100%.

This wide variation in the prevalence of anosognosia shows

that one should always consider the possible effects of the

patient selection, assessment methods used, subtypes of

anosognosia assessed, and assessment times before making

generalizations from the results.

It has been suggested that anosognosia should be studied

in more homogeneous patient groups in order to establish the

true prevalence of anosognosia, since deficits of unawareness

can imply different processes in different patient populations

(Jehkonen et al., 2006a, 2006b; Orfei et al., 2007, 2009;

Starkstein et al., 2010). The frequency and clinical presenta-

tion of anosognosia may vary depending on the side of the

lesion (LH or RH), the timing of the stroke (subacute, acute or

chronic), and the number of strokes (first stroke or recurrent

stroke) (Appelros et al., 2002, 2007; Orfei et al., 2009; Vocat

et al., 2010). In addition, different clinical conditions require

different assessment approaches. This enables establishing

the true nature of anosognosia and helps to givemore targeted

care and rehabilitation to the patients.

Indeedsomeprogresshasbeenmade in thisdirection.During

the past decade 10% of the studies reviewed have assessed

anosognosia in homogeneous groups of LH patients, whereas

this was the case in none of the earlier studies published in

1978e2001. However, the use of patient groups consisting of

patients with either LH or RH damage alone is not enough to

eliminate the variation in the prevalence of anosognosia, since

figureshavealso varied in these studies (inwhich theprevalence

of anosognosia has varied from 17% to 69% in RH patient groups

and from 6% to 46% in LH patient groups).

The timing of the assessment varied widely within patient

groups, which could include patients at the acute, subacute

and chronic stage of stroke. Some studies (Cocchini et al.,

2009; Vossel et al., 2013) acknowledged this and divided their

patients into subgroups based on the time of stroke onset.

This is justified since the prevalence of anosognosia varies

according to the time elapsed since stroke (Starkstein et al.,

2010; Vocat et al., 2010). Furthermore, the reliability of the

methods used in diagnosing anosognosia may vary according

to the time elapsed since stroke. For example, structured in-

terviews inwhich patients are asked about the reason for their

hospitalization or about their difficulties in general are more

adequate for patients at the acute than at the chronic stage of

stroke (Levine et al., 1991; Marcel et al., 2004). This is because

patients at the subacute or chronic phase of illness have


usually received direct or indirect information about the

reason why they are hospitalized and about the difficulties

they can expect to experience during rehabilitation, and

therefore may have learnt the “right” answers to the struc-

tured interview questions about their illness. Therefore, it is

possible thatmore specific questions about abilities in specific

tasks more accurately capture the true essence of unaware-

ness in these patients (Levine et al., 1991; Marcel et al., 2004).

To some extent the variation in the prevalence of anosog-

nosia is also explained by the assessment methods used. It is

difficult to compare the different tests used to evaluate ano-

sognosia: the scales used are different, as are their specificities

and sensitivities. The use of different domain scores probably

helps to give greater accuracy in detecting specific forms of

anosognosia. There is much variation in the type of informa-

tion used in diagnosing anosognosia. The diagnosis of ano-

sognosia can be based on differences between patients’ and

their caregivers’ and/or the clinician’s evaluations, or on dif-

ferences between the patient’s evaluation andhis or her actual

performance. Again it is difficult to compare the information

received from these different sources. There are many poten-

tial sources of error that may affect these assessment

methods: for example, caregivers may underestimate or

overestimate the patient’s condition due to distress or insuf-

ficient information (Prigatano, Borgaro, Baker, &Wethe, 2005).

To conclude, recent studies have concentrated on

describing the phenomenon of anosognosia, its causes and

subtypes, related disorders, prevalence rates, and hemi-

spheric differences. The main focus of research has not shif-

ted very much over the years, but some progress has been

made in terms of gaining a deeper understanding of the

multifaceted syndrome of anosognosia. Observational and

performance-based procedures are nowadays more widely

used in the evaluation of anosognosia to support traditional

interview methods, and modality specificities are also better

taken into account. Patients with language impairment are

now given closer attention following the development of new

assessment methods, and the results are more often obtained

from homogeneous patient groups. The most recent studies

have found that anosognosia for motor impairment is roughly

equally common in both RH and LH groups, which calls into

question the common belief that anosognosia is more com-

mon and more severe in RH lesions.

Recent experimental research findings have also shed light

on various aspects of anosognosia: the pathogenesis of ano-

sognosia, especially concerning motor impairments, different

manifestations of anosognosia at the behavioural level and

possible dissociations of its subtypes. However, the diversity of

assessmentmethods aswell as assessment times between and

within patient groups, and the tendency to use only 1 assess-

ment method to assess the presence of anosognosia are also

seen in the recent studies. Follow-ups also remain rare, and

chronicanosognosiahasbeenevaluatedonly invery rare cases.

A few comments are in order on the limitations of our re-

view. This review was limited to published group studies in

order to examine the assessment of anosognosia in different

stroke populations. This means that some relevant sources of

information such as case studiesmight have been overlooked.

We concentrated on adult subjects sincewewere interested in

the development of the assessment methods of anosognosia.




Q1

Q9

Q2

Q3Q4

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However the presence of anosognosia in subjects under 18

years is an important area of study that can help towards a

deeper understanding of how changing developmental states

may contribute to anosognosia. Among the articles reviewed

were altogether 16 studies, which have probably included

overlapping patient samples (Appelros et al., 2002, 2003, 2003;

Cocchini et al., 2009; Cocchini, Beschin, et al., 2010; Cocchini

et al., 2013; Cocchini, Gregg, et al., 2010; Hartman-Maeir, Sor-

oker, & Katz, 2001; Hartman-Maeir et al., 2002, 2003; Pedersen,

Jorgensen, et al., 1996, 1997; Pedersen, Wandel, et al., 1996;

Starkstein, Fedoroff, Price, Leiguarda, & Robinson, 1992, 1994;

Starkstein et al., 1993). Our review also included studieswhose

primary focus was not to study anosognosia after stroke,

which may have affected the generalizability of our results.

These studies were included in the review because they met

the inclusion criteria and because we wanted to illustrate the

wide range of studies from which the conclusions concerning

the methods of assessment and the prevalence and subtypes

of anosognosias have been drawn. Co-existing disorders (such

as denial, alexithymia, bodily delusions) were not included in

our review. However it is crucial that these co-existing disor-

ders are indeed considered in order to gain a holistic overview

of the prevalence of anosognosia in different patient groups.

Our review offers some recommendations for future

research. First, it is necessary to draw up guidelines for the

selection and number of assessment methods that should be

used in studying different subtypes of anosognosia. Thiswould

go a long way towards improving the generalizability and

comparability of different studies. Secondly, it would be

important to use homogeneous patient samples since deficits

of unawareness can imply different processes in different pa-

tient populations. Therefore findings based on heterogeneous

patient samples can be misleading. Thirdly, the assessment of

chronicanosognosiaand its impactonall theareasofdisability,

not only on basic activities in daily living (ADL), contribute to a

more in-depth understanding of anosognosia. Some of these

recommendations have of course been made earlier, which

only goes to show that anosognosia research is making prog-

ress, but slowly. There is still room for development.

In conclusion, recent studies of anosognosia are more

sensitive to the multifaceted nature of the disorder. This can

be attributed to the efforts invested in developing objective

methods for the assessment of anosognosia, particularly

during the past decade.

Acknowledgements

The study was supported by grants from the Research Fund of

the University of Tampere and the Finnish Cultural Founda-

tion’s the Pirkanmaa Regional Fund.
122123124125126127128129130
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