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59. Cerebrovasc Dis 09

59. Cerebrovasc Dis 09
59. Cerebrovasc Dis 09

R eview

C

erebrovasc Dis 2009;27:280–289 DOI:10.1159/000199466

T

he Evaluation of Anosognosia in Stroke Patients

M.D.Orfei a C. Caltagirone a, b G. Spalletta a, b

a

I RCCS Santa Lucia Foundation and b D epartment of Neuroscience, University of Rome Tor Vergata, R ome , Italy

Introduction A

nosognosia is a self-awareness disorder which pre-vents brain-damaged patients from recognizing the pres-ence or appreciate the severity of deficits in sensory, per-ceptual, motor, behavioural or cognitive functioning,

which are evident to clinicians and caregivers

[1, 2].In particular, anosognosia following stroke

[3]has gained importance for its striking phenomenology, its incidence in the stroke population and because it is detrimental to

the recovery and rehabilitation course

[4–6].Thus,the assessment of anosognosia is fundamental. In fact, mod-ern conceptualizations of awareness deficits in brain-damaged patients highlight the complex and multilevel

nature of these clinical phenomena

[3] . For instance, the pyramidal model proposed by Crosson et al.

[7] hypoth-esizes 3 possible levels of awareness deficits, with specific clinical and rehabilitative implications for each. In the last 30 years, a number of high-quality measures have been proposed, but most of them focus on specific as-pects, leaving other dimensions of anosognosia unex-plored. Thus, at present no single scale is able to fully explore all the components of poor awareness of deficit. This is a relevant issue from a clinical perspective, be-cause a lack of exhaustive diagnostic procedures may po-tentially affect the development of specific and efficient rehabilitation programmes. In addition, heterogeneous selection criteria and assessment modalities contribute to

gather highly variable epidemiological data

[3]and pre-vent a deeper knowledge of awareness processes and im-pairments.

K

ey Words A nosognosia, assessment ? Stroke rehabilitation

Abstract

B ackground: Anosognosia in stroke patients showed a rel-evant detrimental effect on the rehabilitation course and patients’ quality of life, especially in those with brain injury. Although a number of reliable scales for the assessment of anosognosia in stroke and traumatic brain injury have been developed, at present no single measure fully explores the multifaceted nature of the phenomenon. M ethod: A Pub-Med search with appropriate terms was carried out in order to critically review the issue. R esults: The main dimensions to consider in the investigation of anosognosia in brain-in-jured patients are (a) awareness of deficit and related func-tional implications, (b) modality specificity, (c) causal attribu-tion, (d) expectations of recovery, (e) implicit knowledge and (f) differential diagnosis with psychological denial. Time elapsed from stroke, aetiology, laterality, aphasia and clinical complications may influence all these characteristics and must be taken into consideration. Finally, an adequate asso-ciation of the anosognosia evaluation with other neuropsy-chological and behavioural aspects is relevant for a modern holistic approach to the patient.

C onclusions: This review is meant to stimulate the development of a new comprehen-sive assessment procedure for anosognosia in brain injury and particularly in stroke, in order to catch the multidimen-sionality of the phenomenon and to shape rehabilitation programmes suitable to the specific clinical features of every single patient.

C opyright ? 2009 S. Karger AG, Basel R

eceived: December 17, 2007 A ccepted: October 21, 2008 P ublished online: February 6, 2009

T his paper aims to draw attention to a number of is-sues to be considered in the assessment of anosognosia and to encourage the development of new and more ef-ficient diagnostic procedures able to fit modern knowl-edge on awareness phenomena. Thus, on the basis of the recent studies in this area, the most remarkable method-ological issues and specific clinical factors are listed and debated.

F or our purposes, the database was selected using Pubmed Services utilizing the key words ‘stroke’, ‘trau-matic brain injury’ and ‘anosognosia’. The bibliographies of all related articles were searched. All the pertinent lit-erature considered to be of relevant scientific interest by MDO and GS concerning the assessment of diagnosis and severity of anosognosia was selected. We chose a sample of studies, spanning from 1986 to 2007, to exam-ine some salient methodological issues ( t able 1 ).

C lassical versus More Recent Approach to the

Assessment of Anosognosia in Stroke

T he modern concept of anosognosia concerns a mul-tidimensional phenomenon which includes a wider range of related factors. This is quite evident in research on im-paired self-awareness in other medical conditions. For instance, causal attribution of the deficit, evaluation of functional implications in activities of daily living, ex-pectations of recovery, changes in various ability domains (sensorimotor, but also cognitive, behavioural and inter-personal) and adherence to the treatment are part and parcel of the definition of poor awareness of illness in traumatic brain injury (TBI), dementia and schizophre-nia, and as such they are commonly investigated [50]

.In

contrast, these dimensions are mostly disregarded in

stroke, where the best-known questionnaires for anosog-

nosia in stroke, such as Cutting’s questionnaire [51],Bisi-

ach’s Scale [43] , the Anosognosia Questionnaire [8] ,the

Anosognosia for Hemiplegia Questionnaire [52] and the

Structured Awareness Interview [18] , are polarized on

the awareness of sensorimotor deficit per se, consistently

with the original definition of anosognosia [53] . In addi-

tion, the complexity of an awareness deficit is supported

by neuro-anatomic studies, which suggest that anosog-

nosia is due to the impairment of a wide neural net in-

cluding a number of cerebral circuits [54–57] .

T hus, the development of a wider diagnostic perspec-

tive on anosognosia in stroke, consistent with the recent

evolution of the concept of anosognosia, is required. To

date, the measures for anosognosia in stroke, although

quite reliable, are not very diversified, as they are all based

on the clinician’s judgement, provide very similar items Table 1. Studies on anosognosia in relationship to different aetiopathogeneses

and focus on nearly the same few themes. In contrast, in other medical conditions, such as TBI and dementia, more flexible anosognosia trials allow clinicians to mon-itor the evolution of the phenomenon under a number of aspects and also in daily living after discharge. Of course, given proper operational adjustments, the structure of these measures and the general issues they investigate can provide fruitful suggestions to improve the assess-ment of anosognosia in stroke.

Sp ecific Methodological Issues

W hat to Assess?

I n a multifaceted perspective, the main dimensions of anosognosia to investigate are as follows.

M odality Specificity.It refers to the unawareness of specific aspects of the illness but not of others [58].For instance, the patient can be aware of a cognitive deficit but not of a more evident sensorimotor deficit. This is why, unlike present questionnaires for anosognosia in stroke, we suggest the inclusion of a number of specific items to assess the awareness of various deficits, specifi-cally sensorimotor, cognitive, affective and behavioural deficits.

C ausal Attribution.The patient can be aware of the deficit but disregard the real causes, attributing the im-pairment to other factors (e.g. a flu or laziness) or judging the pathological event as less severe than its real nature.

A wareness of Functional Implications, Expectations of Recovery and Need for Treatment.In fact, the patient can admit verbally to suffer from a deficit but not realize its pragmatic consequences, asserting that he/she is capable of doing everything he/she could do before the injury. Also, anosognosic patients can ask insistently to be dis-charged because they are sane [59] or can refuse to attend the rehabilitative programmes and clinicians’ prescrip-tions.

I mplicit Knowledge.This implies an inconsistency be-tween the patient’s verbal answers and behaviours [4, 18].

A frequent contradiction in anosognosic hemiplegic pa-tients is the verbal assertion that they are able to walk but at the same time refuse to leave the wheelchair. Thus, the inclusion of both verbal and non-verbal items is essential to reveal a possible dissociation between explicit and im-plicit knowledge [18, 10, 60] . For instance, with regard to motor deficits, the request to perform some actions, such as to lift the paralysed arm/leg and to compare it with the sound one, to choose between unimanual and bimanual/ bipedal tasks, can be very informative. In fact, an anosog-nosic patient is expected to choose a bimanual task, while an underlying implicit knowledge of the deficit would compel him/her to privilege unimanual tasks [10].Ta-ble 2 points out that 70% of studies on anosognosia in stroke adopted a combined (i.e. verbal and non-verbal) strategy of assessment, although only 29% of them actu-ally required more articulated motor procedures. In or-der to let the implicit knowledge emerge, the alternate use of first/third-person questions about the deficit can also be used. In fact, some anosognosic patients tend to an-swer more correctly when asked to evaluate the deficit as referred to another person than when referred to him/ herself. In the present study, only one study adopting this approach was found [18] . With specific regard to cogni-tive deficits, the patient’s discrepancy between predicted and actual performance in a cognitive task can be very informative, since it does not require any significant in-tervention of others [61, 62] .

C oncurrent Awareness Phenomena.These include ne-glect, confabulations, bodily delusions, misoplegia or anosodiaphoria. Some classical anosognosia scales in-clude items about these issues, but they are generally not sufficiently thorough or discriminating. In particular, the diagnosis of neglect requires attention, given the high co-occurrence with anosognosia and the partial overlap of brain areas involved [20] . Also, it is important to eval-uate the various forms of neglect (e.g. visual, tactile, per-sonal, spatial, extinction) [63] , in order to clarify whether some of them are related to specific dimensions of anosog-nosia and to better define the still debated matter of the co-occurrence of these two phenomena.

D ifferential Diagnosis between Anosognosia and De-nial.This issue should not be undervalued, especially in case of a mild to moderate deficit. At first glance, anosog-nosia and denial produce the same effect, that is the dis-avowal or the minimization of the deficit, but at a deeper analysis some salient behavioural differences emerge [46, 64] .

W ho to Assess?

T he present review stresses a fair variability in the characteristics of the populations considered in different studies. This can account for the high variability in find-ings and makes data hard to compare. In particular, when selecting a sample, the following aspects have to be con-sidered.

M ixed Brain Injury Aetiology.Of the total sample of studies on anosognosia that we considered, 47% recruited only stroke patients, 37% only TBI subjects and 16% com-bined various medical conditions, such as stroke, TBI or

neoplastic pathologies ( t able 1 ). Indeed, data from differ-ent aetiologies, if analysed separately, can be very infor-mative to highlight possible similarities and differences in awareness impairments. In contrast, the study of a het-erogeneous sample can blur data, since in spite of phe-nomenological similarities, unawareness deficits can im-ply very different processes in different patient popula-tions

[50]

.

T ime Elapsed from the Acute Event. Anosognosia can evolve rapidly, within a few days or months and more rarely can last for several years after injury [29, 33, 36, 65].Since anosognosia is more frequent in the acute than in

the chronic phase [51, 66] , the high variability in inci-dence rates

[3] could be partially due to heterogeneous times of testing in different studies. Thus, it is necessary to stress target temporal terms and to discriminate be-tween acute and chronic patients. In addition, these re-quire differential assessment trials, and findings from the two subgroups should be analysed separately. In their

meta-analysis, Pia et al.

[66] defined as acute the patients tested within 29 days after stroke and as chronic those tested after the 30th postinjury day, and found 48% of studies focusing on acute patients, 30% on chronic pa-tients, 9% on both acute and chronic patients, and in 13%

of studies data about time of testing were not available. Given the high and rapid fluctuations of anosognosia in stroke, very acute cases, ranging from 1 to 7 days from injury, should be further discriminated from acute and subacute ones, ranging from 8 to 29 days after stroke. Consistently, in the sample of studies on stroke selected in the present paper, 35% of studies recruited very acute patients only, 25% chronic subjects only, while 40% com-bined subjects with variable time of testing. L aterality of Lesion. I n the present review, most of the studies considered (60%) included patients with both right and left strokes, 35% right only and no study re-cruited exclusively subjects with injury on the left. One study did not report information about laterality of le-sion. Indeed, patients injured on the left can be more dif-ficult to assess because of possible aphasic deficits, so they

tend not to be included

[4, 6, 66, 67] . However, the exclu-sion may cause some confusion due to the underestima-tion of rates of anosognosia in the total brain injury pop-ulation.

A phasia. P atients with global or severe comprehen-sion aphasia cannot be tested on their awareness of lan-Table 2. Characteristics of studies on anosognosia in stroke

guage disorders, but mere behavioural observation can provide information about awareness of sensorimotor deficits. In contrast, productive aphasia can be handled with some specific administration devices. For instance, the clinician can read the answer alternatives aloud and ask the patient to indicate his/her own choice with ges-tures or make him/her fill in the questionnaires on his/ her own. In the present review, 55% of selected studies excluded stroke patients with language disorders, often generally mentioning inadequate linguistic abilities or severe language impairment, while 40% of studies did not mention the issue at all, with a definite loss of informa-tion for the reader.

H ow to Assess?

S ome methodological aspects play a relevant role in the assessment of anosognosia. In particular, differ-ent clinical conditions require different assessment ap-proaches.

P atient Estimation. O bviously, patient estimations of their deficits have to be compared to an objective stan-dard. Clinical judgement is the most frequently adopted criterion in classical anosognosia scales, while awareness questionnaires for TBI and dementia mostly rely upon the direct comparison between patient answers and in-formant/staff reports. In fact, the total difference score, obtained by subtracting patient from caregiver evalua-tions, is supposed to reflect the degree of awareness of the patient. Self/significant other comparisons can be quite informative, due to a daily and long-lasting knowledge of the patient [4] . However, in the acute stage following stroke, this methodology is not fully reliable, since rela-tives and significant others can still have little informa-tion; as well, stress, anxiety [68] and denial coping strat-egy can alter their judgement [4, 33, 69] . In TBI, some measures which specifically examine these aspects have been developed, such as the Revised Patient Competency Rating Scale [68] , a subsequent 3-item addition to the original Patient Competency Rating Scale and the Head Injury Behaviour Scale [69] . Both of them ask the care-giver how stressful the patient’s problematic behaviours are. While recently a trial to test the differential efficacy of various methodologies in anosognosia assessment in dementia has been carried out [70] , to our knowledge an analogous study to determine which approach is more ef-ficient in stroke has not been performed.

C ourse of Anosognosia.Longitudinal studies can be very informative to follow the course of anosognosia that usually evolves as time goes by. In addition, the frequen-cy of assessment has to be rather high, especially in the acute phase. In spite of this, 30% of studies on stroke in-cluded in our review provided a follow-up and, similarly, Jehkonen et al. [71] reported that in 70% of studies no fol-low-up was carried out. However, some pragmatic factors preventing a frequent assessment approach have to be stressed. Firstly, clinical practice and ward routine hard-ly deal with frequent questionnaire administrations, es-pecially in the very acute stage. Analogously, fatigability, patient’s pain and reduced concentration can be salient problems. Thus, in the first days after stroke, assessment should focus strictly on only a few definite issues, not to outwear the subject, and should always explore implicit knowledge of sensorimotor deficits, since the patient may have difficulty in expressing verbally his/her condition. Secondly, early after stroke the patient often has not yet had the chance to put his/her abilities to the test. Analo-gously, questions about functional implications of the deficit can be misleading, and therefore they should be limited. Finally, at this stage, questions about prognosis can be avoided because of the objective lack of informa-tion. In summary, in the acute stage the assessment of awareness deficits has to concern only evident impair-ments, while it can be too early for a reliable self-evalua-tion of cognitive abilities, which can be less salient to the patient than a physical deficit.

S cale Type.Dichotomous scales, such as yes/no or aware/unaware, are not very fruitful, since anosognosia is not an all-or-nothing phenomenon. In contrast, Likert scales seem to be the most appropriate to measure depth of awareness and are adopted in most tools. In addition, separate domain scores should be provided to better highlight possible modality specificities.

A Holistic Approach to Anosognosia

A number of studies showed that awareness of deficits cannot be conceived as an isolated disorder, it must rath-er be integrated in a holistic view of the patient [3, 50]. Thus, in association with the assessment procedure spe-cific to anosognosia, we suggest investigating other con-current dimensions ( t able 3 ): (a) general level of cognitive impairment; indeed, the relationship between anosogno-sia and global cognitive level, as measured for instance by the Mini-Mental State E xamination [81]or Wechsler scales [82] is still controversial, since some authors assert that cognitive impairment is not a causal factor of anosog-nosia, rather a worsening condition[8, 18, 33, 83, 84];

(b) mnestic functions; because anosognosia has been in-terpreted in some studies as the result of a mnestic failure,

Fundamental issues of assessment of anosognosia in stroke

Table 3.

specifically of the inability to integrate new episodic ex-periences into long-term memory or the image of oneself [18, 49] ; (c) language functions. In some studies, phone-mic and semantic abilities in verbal fluency were related to anosognosia [8, 18, 33, 49] , although the nature of this relationship is still unclear; (d) executive functions. The relationship between anosognosia deficits and attention-al control and inhibition function [85] on the one hand, and set-shifting or cognitive flexibility [86] on the other hand, are to be investigated, given their relevance in oth-er self-awareness disorders [33, 49, 87–90] ; (e) psychopa-thology; as it is necessary to ascertain the relationship between anosognosia and neuropsychiatric symptoms. For instance, in anosognosic patients depression and/or anxiety [8, 30, 91] , apathy [92, 93] , anger and hostility [94, 95] and alexithymia [26, 96] require further investigation, given their frequency in stroke patients and their contro-versial role in awareness of illness and patient outcome [24, 30, 46, 49, 64] .

T he administration of these neuropsychological and psychopathological instruments is thought to be neces-sary on the one hand as a diagnostic procedure to de-scribe the complete clinical picture of the patient, and on the other hand to make possible correlations between anosognosia and neuropsychiatric features in stroke pa-tients. In t able 3 , some examples of neuropsychiatric scales validated in stroke patients are given.

F inally, neuro-imaging studies should be part of the diagnostic trial. In fact, a combination of data from con-ventional or, more interestingly, non-conventional mag-netic resonance imaging measures, such as diffusion ten-sor imaging or tractography, with behavioural data, could provide relevant information about brain circuits in-volved in specific dimensions of self-awareness and their deficits, analogously to the investigations carried out in other pathological conditions [97–99] .Currently, these methods are still not completely automated and require the supervision of technical experts. However, despite the time they require, the information they provide may help clinicians to optimize individual rehabilitation pro-grammes in the near future. Also, advanced methods for studying structural indices in the cortex, such as thick-ness, in association with methods for studying function-al activation, permit to follow the process of cerebral plas-ticity following the recovery from awareness deficits [100] . This might explain, if appropriately validated, rea-sons why patients may fully recover within a few hours or may become chronic cases.

Conclusions

A nosognosia represents a stimulating challenge for clinicians, due to its remarkable incidence in stroke pop-ulations [3] , phenomenological variability and effect on the rehabilitation course and the patient’s quality of life. Given the complexity of this phenomenon, similar to oth-er multidimensional fields such as neuropsychology or psychopathology, a reliable assessment procedure for anosognosia is necessary. In spite of their good reliability, present diagnostic questionnaires are not fully exhaus-tive in catching the multifaceted anosognosic phenome-na. In fact, as the model of Crosson et al. [7]illustrates, awareness is not a unitary function, and the deficit can regard different components which can determine im-portant features for the development of a specific reha-bilitation treatment. In addition, anosognosia is no lon-ger conceived merely as the unawareness of a deficit per se but implies a number of related factors, such as attribu-tion, expectations of recovery, psychological denial, need for rehabilitation and estimation of functional limita-tions. Such a wide perspective on anosognosia requires an articulated assessment in order to gain a more definite diagnosis, to develop specific rehabilitation programmes and to understand more deeply awareness and related su-perior neuropsychological processes. Thus, we have out-lined the main dimensions to include them in a flexible and comprehensive assessment procedure for anosogno-sia. Our approach aims to take into consideration the pa-tient in his/her wholeness, in accordance with modern holistic perspectives in medicine, and therefore also in-volves cognitive, neuropsychiatric and behavioural fac-tors.

A nother remarkable issue is the specificity of various clinical situations which require partially different as-sessment modalities. For instance, for acute-phase sub-jects and in general for patients showing vigilance defi-cits, severe cognitive impairment, non-compliance, se-vere language disturbances or behavioural disorders, a more basic set of measures is suitable. Thus, a few instru-ments focusing on awareness of sensorimotor impair-ments, possible implicit knowledge, somatoparaphrenias, global cognitive assessment, language functions and ne-glect could be administered. On the other hand, patients showing persistent anosognosia have to be monitored regularly and as frequently as possible to detect any evo-lution of anosognosia, which in brain-injured subjects can be very sudden. For instance, a very acute-stage ad-ministration, such as within 3 days from stroke, has to be followed by regular consecutive administrations.

A nother frequent problem is represented by aphasia. In our opinion, aphasia should not necessarily be an ex-clusion criterion for the assessment of anosognosia, since in productive and moderate language disorders specific non-verbal assessment methods can be adopt-ed.

I n conclusion, this paper is intended to be a first step towards a more definite, reliable and valid diagnostic methodology, which should be structured ex novo con-sidering the multifaceted expression of anosognosia and the complexity of its interaction with behaviour, cogni-tion and with general clinical aspects.

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