Virtual reality for the assessment of frontotemporal dementia, a feasibility study

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http://informahealthcare.com/idt ISSN 1748-3107 print/ISSN 1748-3115 online Disabil Rehabil Assist Technol, Early Online: 1–5 ! 2014 Informa UK Ltd. DOI: 10.3109/17483107.2014.889230

RESEARCH PAPER

Virtual reality for the assessment of frontotemporal dementia, a feasibility study Mario F. Mendez1, Aditi Joshi2, and Elvira Jimenez3 Disabil Rehabil Assist Technol Downloaded from informahealthcare.com by 68.111.93.227 on 02/14/14 For personal use only.

1

Department of Neurology, Psychiatry & Bio behavioral Sciences, University of California Los Angeles, Los Angeles, CA, USA, 2David Geffen School of Medicine, University of California at Los Angeles, Los Angeles, CA, USA, and 3V.A. Greater Los Angeles Healthcare System, Los Angeles, CA, USA

Abstract

Keywords

Purpose: Behavioral variant frontotemporal dementia (bvFTD) is a non-Alzheimer dementia characterized by difficulty in documenting social-emotional changes. Few investigations have used virtual reality (VR) for documentation and rehabilitation of non-Alzheimer dementias. Methods: Five bvFTD patients underwent insight interviews while immersed in a virtual environment. They were interviewed by avatars, their answers were recorded, and their heart rates were monitored. They were asked to give ratings of their stress immediately at the beginning and at the end of the session. Results: The patients tolerated the head-mounted display and VR without nausea or disorientation, heart rate changes, or worsening stress ratings. Their insight responses were comparable to real world interviews. All bvFTD patients showed their presence in the VR environment as they moved their heads to face and respond to each avatar’s questions. The bvFTD patients tended to greater verbal elaboration of answers with larger mean length of utterances compared to their real world interviews. Conclusions: VR is feasible and well-tolerated in bvFTD. These patients may have VR responses comparable to real world performance and they may display a presence in the virtual environment which could even facilitate assessment. Further research can explore the promise of VR for the evaluation and rehabilitation of dementias beyond Alzheimer’s disease.

Frontotemporal dementia, insight, virtual reality History Received 10 November 2013 Revised 27 January 2014 Accepted 27 January 2014 Published online 14 February 2014

ä Implications for Rehabilitation   



Clinicians need effective evaluation and rehabilitation strategies for dementia, a neurological syndrome of epidemic proportions and a leading cause of disability. Memory and cognitive deficits are the major disabilities and targets for rehabilitation in Alzheimer’s disease, the most common dementia. In contrast, social and emotional disturbances are the major disabilities and targets for rehabilitation in behavioral variant frontotemporal dementia (bvFTD), an incompletely understood non-Alzheimer dementia. Virtual reality is a technology that holds great promise for the evaluation and rehabilitation of patients with bvFTD and other non-Alzheimer dementias, and preliminary evidence suggests that this technology is feasible in patients with bvFTD.

Introduction Behavioral variant frontotemporal dementia (bvFTD) is a common dementia among those who are 65 years or younger. This neurodegenerative syndrome, previously widely known as ‘‘Pick’s disease’’, differs strikingly from Alzheimer’s disease (AD) in that its defining manifestations are changes in social and emotional behavior [1]. Patients with bvFTD present with socioemotional disengagement, loss of empathy, violations of social norms, or even sociopathic acts [2]. These changes result from

Address for correspondence: Mario F. Mendez, MD, PhD (Neurobehavior), (691/116AF), V.A. Greater Los Angeles Healthcare Centre, 11301 Wilshire Blvd, Los Angeles, CA 90073, USA. Tel: +31 04783711 x42696. E-mail [email protected]

circumscribed atrophy of anterior parts of the frontal lobes and adjacent anterior temporal regions, usually with either tau or TDP-43 positive neuronal inclusions [3]. Clinically, this neuropathology begins in key frontotemporal areas involved in socialemotional behavior, which forms a hub for the ‘‘Salience Network’’, or the neural network involved in the ‘‘Social Brain’’ [4]. Despite the central importance of social-emotional changes in bvFTD, there are barriers in documenting them. Social-emotional interactions are difficult to assess in brief, contrived, and controlled clinical settings, and patient reports are unreliable because these patients have impaired insight into their disease [5]. Moreover, patients with non-AD dementias with frontal lobe involvement often lack initiative or have ‘‘abulia’’, and this lack of verbal or non-verbal behavior and responses otherwise impairs the ability to evaluate the extent and range of their disturbed

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behavior. These barriers to documenting and characterizing their social-emotional disturbances impede the development of rehabilitation strategies targeted at bvFTD. Virtual reality (VR) technology may be an answer to the problem of evaluating disturbed behavior in bvFTD and other non-AD dementias. With the application of VR, it is possible to elicit and examine the patient’s actual interpersonal behavior and responses to avatars while manipulating the social-emotional environment. The immersion of bvFTD patients in a virtual environment also allows the exploration of potential rehabilitation strategies for dealing with their social-emotional changes. For these reasons, VR may be particularly ideal for evaluating patients with bvFTD. Investigators are already using VR through a range of real world social settings such as work, street, parks, and even a supermarket in the related conditions of mild cognitive impairment (MCI) and AD [6]. There has been very little work, however, on the application of VR technology to non-AD dementias like bvFTD, and questions remain as to whether VR is feasible in these patients. It is unclear if VR is too complex and difficult to use in older patients or those with dementia [7], whether they are prone to nausea and other side-effects from wearing a head-mounted display (HMD), and whether they attain sufficient ‘‘presence’’, or the experience of being in the virtual environment [8], for the use of VR to be successful [9]. As an initial step to the application of VR to the socialemotional changes of bvFTD, we assess the feasibility of placing patients with this unique dementia in a virtual environment [10]. This pilot study evaluates whether these behaviorally disturbed patients tolerate the paraphernalia and procedures of VR and have sufficient presence in the virtual environment. This pilot research investigates VR in bvFTD through a program that assesses the most easily tested feature of bvFTD, their loss of insight [11].

Methods Subjects Five patients with bvFTD from a large university-based clinical program were enrolled in this Institutional Review Boardapproved study. The patients met diagnostic criteria for probable bvFTD after an evaluation involving clinical, neuropsychological and neuroimaging assessments [1]. These diagnostic criteria emphasized on dis-inhibition, apathy, loss of sympathy or empathy, repetitive behaviors, and dietary changes and were supported by predominant frontal or anterior temporal changes on magnetic resonance or positron emission tomography imaging. Other inclusion/exclusion criteria included the absence of aphasia or complicating medical or psychiatric illnesses and medications such as psychotropic drugs. In a testing session preceding VR, these patients were further characterized for severity of dementia, frontal lobe functions, and insight questions with a structured interview and a verbal measure of fluency of communication. Severity was further assessed with the Mini-Mental State Examination (MMSE) [12], the Clinical Dementia Rating Scale (CDR) [13], and the Functional Activities Questionnaire (FAQ) [14]. Frontal lobe functions were evaluated with the Frontal Assessment Battery (FAB) [15], the Frontal Systems Behavior Scale (FrSBe) [16], and the Wisconsin Card Sort Test (WCST) [17]. Finally, they underwent the UCLA structured Insight Interview [5], administered by single researcher in real life. Their verbal fluency was then tested with mean length of utterance (MLU) in morphemes [18], a language measure that could be accurately compared across real world and virtual reality samples independent of time length for questioning, latency of responses or pauses, and other, mostly temporal variables.

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Apparatus During the lab session, the participants sat in a chair placed over a bass shaker or tactile transducer, a device that transmits the feel of sound. They wore an eMagin Z800 HMD (Virtually Better Co., Atlanta, GA) that included separate display screens for each eye, integrated head-tracking and stereo earphones. During the VR procedure, the participants underwent continuous psycho-physiological monitoring for heart rate (HR). The HR was measured using BioHarness 3.9 (Biopac Inc., Goleta, CA), an elastic band around the sternum which made a skin contact and transmitted the HR signal. Virtual environment The participants were immersed in an environment consisting of a conference table with five adults (three males and two females) (modified from Virtually Better). The people around the table appeared initially busy (one reading a newspaper, others talking), then would quiet down in order to start the meeting. The avatars were non-threatening individuals, similar to those encountered working in the healthcare field. The participants were seated in a chair at the end of the conference table and told that they would be interviewed by the five avatars. They were asked to answer their questions as if they were real people. The avatars asked a series of questions, one at a time, comprising a subset from the UCLA Insight Interview on cognitive insight (awareness of having a disorder) and emotional insight (concern over having a disorder) [5]. As the participant responded, the avatars gave positive or negative feedback through nodding or shaking their heads. Outcome variables During the VR session, the participants were observed for head turning towards the speaking avatar and readiness to verbally respond. Their verbal responses were audio-recorded and later transcribed for analysis. The responses were categorized for initial yes/no response and analyzed for MLUs, similar to a pre-VR real world intake analysis. Both immediately pre-VR session and postVR session, the participants were asked to self-report their levels of arousal, stress, anxiety, anger, fatigue, and attention using a short, standardized Likert-scale questionnaire. They were also asked to describe any problems with their VR experience, and whether they had any physical discomforts. HR analysis employed the Biopac Acqknowledge program to determine intra-subject differences in HR between baseline (pre-question) and stimulus (7 s post-question) conditions.

Results The five patients who participated included two men and three women with a mean age of 56 SD 12.8 years, disease duration of 3.0 SD 1.6 years, and education of 16 SD 3.2 years. Additional characteristics are as seen in Table 1. For the insight questionnaire, the patients’ VR insight responses (percent ‘‘Yes’’ answers) were compared to a published cohort with bvFTD (44% versus 33%; 2 ¼ 0.72, non-significant), but differed from a published AD sample (44% versus 74%; 2 ¼ 6.04, p50.05) [5]. In other words, the bvFTD patients displayed a lack of insight during VR, with the majority of questions answered ‘‘No’’ regarding both knowledge and concern over having a disorder. However, the bvFTD patients endorsed more problems related to their disease in the VR environment compared to their real world answers to the same insight questions, i.e. they changed six ‘‘No’’ answers (e.g. ‘‘I don’t have a problem’’) to ‘‘Yes’’ answers, although one patient went from ‘‘Yes’’ to ‘‘No’’ on three questions. All patients clearly were engaged with the avatars, turning their heads and looking at each one as they asked questions.

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DOI: 10.3109/17483107.2014.889230

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Table 1. Characteristics of bvFTD participants (n ¼ 5). Measure Mini-Mental State Examination Clinical Dementia Rating Score Functional Activities Questionnaire Frontal Assessment Battery Frontal Systems Behaviour Scale-BEFORE Frontal Systems Behaviour Scale-AFTER Wisconsin Card Sorting Test Errors Mean Length of Utterances-Real World Mean Length of Utterances-Virtual World

Scores 21.3 1.0 21.5 11.0 81.3 152.3 33.2 0.2 6.8

SD SD SD SD SD SD SD SD SD

7.3 0.0 2.9 5.2 17.7 33.0 10.6 0.4 5.1

Interpretation Mild Dementia (cut-off of 23) Mild Dementia (normal ¼ 0) Requires some assistance (max ¼ 30) Mild impairment (cut-off of 12) Normal Abnormal, 42 SD below mean) T-Scores 42.5 SD below mean Significantly greater (t ¼ 2.89, p50.05)

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The Frontal Systems Behaviour Scale is completed by caregivers. BEFORE ¼ retrospective evaluation prior to dementia and AFTER ¼ current status.

Figure 1. Mean Stress Symptom Rating Questionnaire responses, Pre-VR session and Post-VR session. Light bars are Before Ratings and dark bars are After Ratings for the six patients. The bars include standard error bars.

The patients responded to all questions, showing that they were engaged. Compared to their real world insight interview, the patients were more talkative and gave more elaborate answers with details when questioned by the avatars, as evidenced by analyses of the transcripts and larger MLUs for responses in VR (6.80 SD 5.07) compared to in the real world (0.22 SD 0.38); t ¼ 2.89, p50.05. None of the patients endorsed in any physical complaints or discomforts with VR. The mean heart rate increase was only 2.67 SD 1.37 beats per minute for VR versus baseline. There was no significant post-VR versus pre-VR side-effects on the Likert-scale questionnaire as seen in Figure 1.

Discussion This pilot study shows the feasibility of conducting VR work with patients with bvFTD, a common non-AD dementia with onset in middle life. All patients tolerated the procedure well, including wearing the HMD, and there were no side-effects. The bvFTD patients showed presence in the virtual environment as they moved their heads to face and answer the avatars’ questions. An unexpected finding was the presence of greater interaction, and elaboration of comments, with the avatars in the VR environment, than with real people on the non-VR evaluation. Investigators are increasingly using VR in neurological conditions, including AD dementia and MCI, both for assessment and rehabilitation. They have used VR for screening and assessment of memory and visuospatial changes in patients

suspected of AD dementia and MCI [19]. VR has been used to characterize their episodic memory [20], spatial learning and navigation [21,22], and functional status [10,23]. In these populations, VR has also been used for rehabilitation as memory-training programs [24], spatial navigation and route or 3-D environmental learning [25,26], and functional enhancement or enhancement of activities of daily living [7]. In AD and related neurological conditions, VR has proven effective in generalizing the symptoms and therapeutic interventions in the VR environment to the real world, particularly in the visuospatial domain [20,21,25,26], and, although needing further replication, the results of memory training in the VR environment appear very promising [24]. In addition, VR has been feasible in other neurological disorders for the rehabilitation of motor symptoms, including Parkinson’s disease [27], cerebral palsy [28], stroke [29,30] and multiple sclerosis [31]. In contrast, VR has rarely been applied to the assessment and rehabilitation of patients with non-AD dementias. There is one prior VR study in ‘‘Pick’s disease’’ showing topographical memory impairment for items in a complex VR town; however, on review, the patient did not have the clinical syndrome bvFTD [32]. It is time to significantly extend VR technology to the non-AD dementias. VR can target the social-emotional behaviors that occur in bvFTD and in some other non-AD dementias. Investigators have shown VR to be useful for evaluating and promoting socialemotional behavior in subjects with schizophrenia [33], autism [34], and traumatic brain injury [35], as well as adolescents [36]. Recently, studies have shown that VR is valuable for the investigation of sophisticated high-level social behaviors [37], including empowering pro-social behavior [38], assessing the role of proxemics and social salience [39], and assessing the influence of imitation on social influence [40]. Hence, it is reasonable to apply VR to the assessment and rehabilitation of social-emotional behavior among patients with bvFTD and related frontallypredominant dementias. An unexpected finding from this pilot study was that VR facilitated verbal interaction from the bvFTD patients. Contrary to the concern that they might not attain sufficient presence in the virtual environment, the bvFTD patients had no difficulty being and responding in the imaginary world [41]. Compared to a nonVR clinical interview, the patients were more talkative and gave more elaborate answers when questioned in VR by multiple interviewers in a formal interview setting. The reason for this is unclear, but it may reflect an unchallenged sense of presence, or engagement, in the virtual environment [41]. In other words, dementia patients usually have the basic layers of presence, the sense of how their body moves in the virtual environment and an integrated perception of their experience [9,23]. This basic presence is automatic, intuitive, and impressionistic, and is normally followed by analysis and questioning of its reality,

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context, and meaning [8,9,42]. In bvFTD and other frontal lobe disease, there is a known absence of an impulse or trigger for critical appraisal due to disturbance of the ventromedial prefrontal region [43]. Patients with bvFTD or with frontal lobe disease may not analyze the VR experience further and may continue in an unchallenged impressionistic mode without a dilemma arising around its imagined nature. There were, of course, limitations to this pilot study. First of all, it is a feasibility study, meant to evaluate the safety and tolerability of VR in this non-AD dementia. Hence, the number of subjects was small and limits conclusions on the insight interview results. Second, it was not a controlled study, and no conclusions can be reached about performance differences from normal subjects, particularly in regards to facilitating verbal output in this virtual environment. Nevertheless, although preliminary, this pilot data indicates the need to investigate further whether VR can facilitate social-emotional behavior among patients with bvFTD. In conclusion, VR is feasible for patients with bvFTD and may have advantages, including the possibility of facilitating their social-emotional behavior within the virtual environment. The similarity between the qualitative results of the insight interview in real world and VR conditions suggests that the VR environment is at least comparable to a clinical, in-person interview. The findings of facilitated behavior are tentative and must be replicated, but, it is clear that VR environments can be safely extended for the documentation and rehabilitation of the behavioural disturbances that characterize patients with bvFTD and, possibly, other non-AD dementias.

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9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20.

Acknowledgements Authors thank Michelle Mather for her assistance in conducting this project.

21.

Declaration of interest

22.

The authors report no conflicts of interest. The authors alone are responsible for the content and writing of this article. This work was supported by NIH funding from NIA #R01AG034499-04.

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