Visual verticality perception after stroke: A systematic review of methodological approaches and suggestions for standardization

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Visual verticality perception after stroke: A systematic review of methodological approaches and suggestions for standardization C. Piscicelli a,b,*, D. Pe´rennou a,b a

De´partement de re´e´ducation neurologique, CHU de Grenoble, Grenoble, France Laboratoire de psychologie et neurocognition CNRS UMR 5105, Grenoble-Alpes universite´, clinique de me´decine physique et re´adaptation, CHU de GrenobleAlpes, 38034 Grenoble, France

b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 30 November 2015 Accepted 7 February 2016

Objective: Visual vertical (VV) measurements are being increasingly used for routine clinical assessment of spatial cognition, to investigate otolithic vestibular function and identify altered verticality perception as a possible cause of postural disorders after stroke. The objective of this paper was to synthesize knowledge of assessment methods for testing VV after stroke. Methods: This systematic review, following the PRISMA statement, involved a search for articles in MEDLINE via PubMED published up to November 2015 by using the search terms ‘‘visual vertical,’’ ‘‘verticality perception’’ and ‘‘stroke’’. We included only case or group studies on VV perception after hemispheric, brainstem or cerebellar strokes. Two authors independently assessed data on patients’ and VV assessment characteristics, outcome measures, ranges of normality and psychometric properties. Results: We assessed reports for 61 studies (1982 patients) of VV for hemispheric (n = 43), brainstem (n = 18) or cerebellar (n = 8) stroke. VV assessment procedures varied widely in paradigm, type of stimulus, patient posture, number of trials and outcome measures. However, on the basis of recent studies it is recommended assessing VV in absolute darkness, with an even number of trials, from 6 to 10, with the body maintained upright. Under these conditions, normal VV orientation (mean of VV estimates) can be considered from 2.58 to 2.58 and is highly reliable for use in clinical practice and research. A difference  28 between repeated measures for a given patient can be interpreted as a real change in VV perception. Myriad of protocols have been proposed, for which psychometric properties must be better analyzed. Conclusions: This first review of VV assessment methods after stroke shows a great heterogeneity of procedures, settings and parameters, among which only some are eligible for standardization to limit measurement errors and better interpret the results. ß 2016 Published by Elsevier Masson SAS.

Keywords: Visual vertical Spatial cognition Stroke hemisphere Brainstem Cerebellar Psychometrics

1. Introduction The visual estimation of the vertical (visual vertical, VV) is the most common test used to assess verticality perception in research and clinical practice. This measure provides information about the vestibular contribution to spatial cognition. The recent evolution of knowledge on balance disorders in neurological diseases, especially after stroke [1], has progressively led to this test being integrated into routine assessments after brainstem [2–5] or hemispheric stroke [6–8] to better understand the specific role played by an altered internal model of verticality as a potential * Corresponding author at: Laboratoire de psychologie et neurocognition CNRS UMR 5105, Grenoble-Alpes universite´, clinique de me´decine physique et re´adaptation, CHU de Grenoble-Alpes, 38034 Grenoble, France. E-mail address: [email protected] (C. Piscicelli).

cause of balance disorders. Therefore, the measurement is useful to guide rehabilitation [1] and to follow recovery [6,7]. Patients with a biased reference of verticality should benefit from a specific rehabilitation program of lateropulsion and postural disorders, aiming to recalibrate their internal model of verticality [1]. The VV perception test consists of adjusting a luminous line to the vertical in darkness. This simple test requires sufficient visual capacity to perceive and align the luminous stimulus to the vertical. VV does not assess the visual contribution to the internal representation of verticality. In contrast, during the assessment, all visual orientation cues in the environment are suppressed and subjects are tested in absolute darkness. The VV perception test assesses mainly the contribution of the vestibular graviception to the construction and updating of the sense of verticality [1]. Thus, the VV test is considered the reference to investigate vestibular otolithic function [9–12], and one clinical sign of a

http://dx.doi.org/10.1016/j.rehab.2016.02.004 1877-0657/ß 2016 Published by Elsevier Masson SAS.

Please cite this article in press as: Piscicelli C, Pe´rennou D. Visual verticality perception after stroke: A systematic review of methodological approaches and suggestions for standardization. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/ j.rehab.2016.02.004

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2. Methods 2.1. Study selection and data collection We searched for articles published in English, with no limitation on publication date, in MEDLINE via PubMed (last search on November 4, 2015) with the search terms ‘‘visual vertical’’ or ‘‘verticality perception’’ and ‘‘stroke’’, regardless of the nature of articles. We also consulted experts in the field and handsearched the reference lists of identified articles. The systematic review followed the PRISMA statement [25,26]. Eligibility criteria included group or case studies on the visual perception of verticality in stroke patients of any age and any lesion location (brainstem, hemispheric and cerebellar). Studies of patients with brain neurodegenerative lesions or traumatic lesions were excluded. Two reviewers (CP and DP) independently assessed the eligibility of articles on the basis of the titles and abstracts in an unblinded standardized manner, then the full-text articles were retrieved. Any disagreements were resolved by consensus. One author (CP) extracted the following data from studies by using a data extraction form, and the second author (DP) checked the extracted data. Disagreements were resolved by discussion. Data were extracted on characteristics of patients, including lesion side

and localization, and post-stroke delay; characteristics of VV assessment, including patient postural setting, the test stimulus, type of paradigm, task, response modality and number of trials; outcome measures; ranges of normality used or defined; and psychometric properties. 3. Results 3.1. Study selection and characteristics

Screening

Idenficaon

The flow diagram for study selection is presented in Fig. 1. The electronic search returned 142 citations. Hand searching identified 26 additional eligible articles. After eliminating duplicates and articles considered not meeting the selection criteria, we examined articles for 61 studies (58 group studies and 3 case studies; 1982 patients). Selected studies were published from 1970 to 2015, with increasing frequency over time, from one study in both the 1970s and 1980s to 9 studies in the 1990s, 23 in the 2000s and 27 in the 2010s (Fig. 2).

142 arcles idenfied by database searching14

26 arcles idenfied by other sources

143 arcles aer discarding duplicates

75 arcles excluded 68 arcles screened

Eligibility

vestibular tone imbalance in the roll plane is the tilt of the VV perception, whereas the other modalities of verticality perception (postural, haptic) are not impaired in peripheral vestibular dysfunction. The direction of VV tilt (ipsilesional versus contralesional) depends on the lesion location and thus helps with the topographic diagnosis. Peripheral and central pontomedullary brainstem lesions cause large ipsilesional VV tilts due to ocular torsion induced by asymmetrical tonus in torsional vestibulo-ocular pathways [2–4,12]. Upper brainstem lesions, pontomesencephalic, more often cause contralesional than ipsilesional VV tilts because of the decussation of the vestibular tracts from the vestibular nuclei to the vestibular cortex via the thalamus [3,5,13–15]. In hemispheric lesions, VV perception is mainly contralesionally biased, although ipsilesional VV tilts may also be found. These ipsilesional VV tilts are less frequent, found in about 10% of patients [3,8,16–19] and are smaller in magnitude and their cause remains to be clarified. Patients with hemispheric stroke and ipsilesional VV tilt never show ipsilesional tilt of the postural vertical [8]. With their low frequency, small magnitude and non-congruency with postural vertical tilts, ipsilesional VV tilt may depend on underlying mechanisms different from those involved in contralesional VV tilts after hemispheric stroke. In a series of 117 patients with subacute hemisphere stroke, we showed that patients with contralesional (n = 48) and ipsilesional (n = 17) VV tilt differed in lesion side, with more right-sided lesions in patients with contralesional tilt and no hemispheric predominance in those with ipsilesional VV tilt [18]. Ipsilesional tilts did not seem to be a lateralized phenomenon, as compared with the dominance of the right hemisphere with contralesional VV tilt in this study and more generally for spatial cognition. In cerebellar stroke, contralesional [20–24] and ipsilesional [20–23] VV tilts have been described. The lesion of specific structures might determine the direction of the VV tilt. For instance, the lesion of the dentate nucleus is associated with contralesional VV tilt, but the dentate nucleus is spared in ipsilesional VV tilt [20,21]. The VV test is increasingly being used in the clinic after stroke, but standardized assessment and a better knowledge of the psychometric properties are needed. Indeed, the methodological approaches of the myriad protocols used vary widely. We conducted a systematic review of the literature on VV perception assessment after stroke to synthesize knowledge of the methodologies used and to propose recommendations for standardization.

Included

2

61 full-text arcles assessed for eligibility

- Not a visual vercality percepon study

7 full-text arcles excluded - Literature synthesis (n=6) - Degenerave lesion (n=1)

61 studies included in qualitave synthesis

Fig. 1. Flow of studies in the review.

Fig. 2. Frequency of studies of visual vertical (VV) after stroke published over the years, expressed in decades.

Please cite this article in press as: Piscicelli C, Pe´rennou D. Visual verticality perception after stroke: A systematic review of methodological approaches and suggestions for standardization. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/ j.rehab.2016.02.004

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Table 1 Stroke location, post-stroke delay, lesion side, number of patients and controls, types of paradigms and outcome measures reported in the 61 selected studies of visual vertical (VV) perception after stroke. Authors

Date

Lesion side

Post-stroke delay

Hemisphere strokes Friedman [27] Choy [28]

1970 1980

– 14 L/26 R

Dieterich and Brandt [10] Brandt et al. [3]

1993 1994

– –

Kerkhoff and Zoelch [29]

1998

14 L/27 R

– Subacute and chronic Acute Acute and subacute Subacute and chronic

Anastasopoulos and Bronstein [31] Anastasopoulos et al. [30] Kerkhoff [32]

1999

–

Chronic

1999 1999

– –

Karnath et al. [33]

2000

0 L/10 R

Yelnik et al. [16]

2002

Saj et al. [34–36]

Number of controls

Paradigm

VV Orientation

VV Uncertainty

67 40

– 22

– –

NE NE

35 71

– –

Hemispheric dome Hemispheric dome

Mean Absolute mean Mean Mean

41

12

Constant errors

Difference threshold

1

22

Computerized ‘‘visualspatial perception’’ program –

Mean

NE

– Subacute and chronic

8 34

20 22

Mean Constant errors

NE Difference threshold

10

5

Mean

NE

20 L/20 R

Acute and subacute Subacute

– Computerized ‘‘visualspatial perception’’ program –

40

20

–

Mean

2005 2005 2005 2006

0 L/8 R 0 L/8 R 0 L/16 R 17 L/13 R

Subacute Subacute Subacute Subacute

8 8 16 30

6 4 6 –

Visuo-haptic vertical Visuo-haptic vertical Visuo-haptic vertical –

Mean Mean Mean Absolute mean

2006

13 L/17 R

Subacute

30

20

–

2006

14 L/16 R

Subacute

30

23

Rod and frame test

Johannsen et al. [39] Saj et al. [40] Bonan et al. [7]

2006 2006 2007

2 L/13 R 0 L/12 R 14 L/14 R

Acute Subacute Subacute

15 12 28

10 8 20

– Visuo-haptic vertical –

Lafosse et al. [41] Barra et al. [42] Pe´rennou et al. [8] Barra et al. [43] Barra et al. [44]

2007 2008 2008 2009 2010

13 L/16 R 6 L/9 R 26 L/54 R 9 L/13 R 9 L/14 R

Subacute Subacute Subacute Subacute Subacute

37 15 86 22 23

8 12 33 – 27

– – – – –

Absolute mean Absolute mean Mean Mean Absolute mean Mean Mean Mean Mean Mean

Maximum difference CWCCW biases NE NE NE Maximum difference CWCCW biases Standard deviation NE

Funk et al. [45]

2010

8 L/16 R

Subacute and chronic

24

8

Constant errors

Funk et al. [46]

2011

12 L/24 R

Subacute

36

12

Paci et al. [47]

2011

4 L/4 R

8

10

Tarnutzer et al. [22]

2011

–

6

7

Tesio et al. [48] Utz et al. [49]

2011 2011

2 L/1 R 0 L/34 R

Acute and subacute Acute and subacute Subacute Subacute

Computerized ‘‘visualspatial perception’’ program Computerized ‘‘visualspatial perception’’ program –

3 34

Baier et al. [15,17,50]

2012 2012 2012

28 L/38 R 22 L/32 R 17 L/15 R

Acute Acute Subacute

Rousseaux et al. [54] Braem et al. [55] Mansfield et al. [56] Oppenla¨nder et al. [57]

2013 2013 2013 2014 2015 2015

13 L/14 R – 0 L/42 R 0 L/16 R 4 L/10 R 0 L/24 R

Piscicelli et al. [18,19]

2015

Bonan et al. [6,37,38]

Saeys et al. [51] Baier et al. [52,53]

Rousseaux et al. [59]

Number of patients

NE NE

NE NE Standard deviation NE NE NE NE Standard deviation Difference threshold

Constant errors

NE

VV Bias

Threshold

–

Mean

22 16

– –

66 54 32

– – –

Hemispheric dome Hemispheric dome

Acute – Subacute Subacute Chronic Subacute

27 10 42 16 14 24

– – – 29 10 –

23 L/23 R

Subacute

36

20

Hemispheric dome Hemispheric dome Visuo-haptic vertical – – Computerized ‘‘visualspatial perception’’ program –

Mean Absolute mean Mean Mean Absolute mean Mean Mean Mean Mean VV error Constant errors

Standard deviation Absolute error NE

2015 2015

60 L/57 R 8 L/12 R

Subacute Subacute

117 20

– –

– –

Mean Mean

2015

0 L/46 R

Subacute

46

–

Visuo-haptic vertical

Mean

Mean

NE NE NE NE NE NE NE NE Difference threshold Standard deviation NE Standard deviation Standard deviation

Please cite this article in press as: Piscicelli C, Pe´rennou D. Visual verticality perception after stroke: A systematic review of methodological approaches and suggestions for standardization. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/ j.rehab.2016.02.004

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4 Table 1 (Continued) Authors

Date

Lesion side

Post-stroke delay

Brainstem strokes Friedman [27] Brandt and Dieterich [12]

1970 1992

– –

Dieterich and Brandt [10]

1992

–

Bronstein et al. [4] Dieterich et al. [60] Cnyrim et al. [61]

1993 2003 2005 2007

– – – 24 L/26 R

– Subacute and chronic Acute and subacute Acute – – Subacute

Yi et al. [14]

2007

4 L/4 R

Pe´rennou et al. [8] Baier et al. [20] Zwergal et al. [62] Tarnutzer et al. [22]

2008 2009 2009 2011

– 29 L/27 R – –

Tesio et al. [48] Baier et al. [50] Frise´n et al. [63] Kim et al. [64] Yang et al. [5] Choi et al. [65]

2011 2012 2012 2014 2014 2015

2 L/1 R 46 L/33 R – 6 L/6 R – –

Kim et al. [66] Tarnutzer et al. [22]

1970 2008 2009 2009 2011

– 10 L/13 R 29 L/27 R 6 L/3 R/5 Bilateral –

Frise´n et al. [63] Choi et al. [23] Tarnutzer et al. [24]

2012 2014 2015

– – 0 L/1 R

Cerebellar strokes Friedman [27] Baier et al. [20,21]

Subacute and chronic Subacute Acute Acute Acute and subacute Subacute Acute – – Acute Acute

– – Acute Acute Acute and subacute – Acute Acute

Number of patients

Number of controls

Paradigm

VV Orientation

VV Uncertainty

67 95

– –

– Hemispheric dome

Mean Mean

NE NE

36

–

Hemispheric dome

Mean

NE

110 20 – –

Hemispheric dome – Hemispheric dome Hemispheric dome

NE NE NE NE

8

20

–

Mean Mean Mean Absolute mean Mean

86 56 12 6

33 – 30 7

– Hemispheric dome Bucket test –

Mean Mean Mean Mean

3 79 35 12 82 6

22 – 10 – – –

– Hemispheric dome Bucket test – – –

Mean Mean Mean Mean Mean Mean

NE NE NE Standard deviation Absolute error NE NE NE NE Standard deviation/ mean

67 31 56 14 6

– – – – 7

– Hemispheric dome Hemispheric dome – –

Mean Mean Mean Mean Mean

35 27 1

10 51 11

Bucket test – –

Mean Mean Mean

111 2 3 50

NE

NE NE NE NE Standard deviation NE NE NE

Data are presented by stroke location (hemisphere, brainstem and cerebellar). L: left-sided lesion; R: right-sided lesion; NE: not estimated. For the section ‘‘paradigm’’, only the paradigms detailed in the Section 3 ‘‘Type of paradigm’’ were specified; the others were missing or corresponded to homemade protocols.

3.2. Characteristics of stroke patients In total, 43 articles reported VV perception after a hemispheric stroke [3,6–8,10,16–19,22,27–59], 18 after a brainstem stroke [2,4,5,8,12–15,21,22,27,48,60–65]; only 3 articles related to Wallenberg syndrome [2,60,61] and 8 cerebellar lesions [20–24, 27,63,66] (Table 1). VV perception was mainly assessed at acute (n = 19 studies) [2,3,5,10,13,15,17,21–24,33,39,47,50,52,62,65,66] or subacute stages (n = 37) [2,3,6–8,12,14,16,18,19,22,28,29,32– 38,41–49,51,54,55,57–59,61] and less frequently at chronic stages (n = 8) [12,14,28,29,31,32,45,56]. These data were missing for 8 studies. Studies of hemispheric stroke mostly involved unilateral lesions; some assessed only right-sided hemisphere lesions [24,33–36,40,49,54,55,57,59]. 3.3. Characteristics of VV assessment procedures 3.3.1. Patient postural setting In all studies, patients were in the sitting position. The seated position is safe, comfortable and allows for assessing all patients, even those who could not stand alone. However, in some studies, the position of the trunk and head were free [4,16,23,27,28,31,33,37–39,41,48,51,62–64], whereas in other studies, the head was maintained in a fixed upright position by a chinrest [2,3,5–7,10,12–15,17,20–22,24,29,32,45–47,50,52,53, 55,57,60,61,65,66] or both the trunk and the head were maintained upright [8,18,19,30,34,36,40,42–44,49,54,56,59]. This question is critical for stroke patients given their frequent postural disorders, especially spontaneous lateral whole body inclination, which may

compromise their ability to sit on their own, and induce the wellknown impact of body tilt on verticality perception. Indeed, a recent study revealed that postural setting had a major impact on VV measurements in patients with postural disorders who were unable to sit [58]. In these patients, maintaining the trunk and the head upright enhances the validity of VV orientation and uncertainty (Fig. 3). Measuring VV without any body maintenance is valid only for participants with satisfactory balance abilities. Besides ensuring the validity of the measurement in stroke patients with postural disorders, maintaining the body upright has the advantage of standardizing the VV assessment conditions between patients and in the same patient between repeated measures. Such a standardization of postural settings would allow for comparing estimates of a given patient relative to the reference population with which the standards have been established, a comparison with itself in the context of repeated measures for follow-up, and comparing results between studies in the clinical research setting. 3.3.2. Characteristics of the test stimulus The visual stimulus could be a metal or plastic luminescent rod [2–4,10,12,13,15,17,20,21,49,50,52,53,60,61], a metal rod with lighted leads [34–36,40,54,55,59] or a luminous line presented on a computer screen [5,8,16,18,19,23,29,32,33,39,41–46,48,57,58, 64,65] or projected on a wall [7,22,24,30,51,56]. We identified two types of paradigms: a mechanical VV assessment procedure and an electronic procedure. This latter procedure has the advantage of an automatic computerization of the data without the intervention of the investigator, thereby allowing for fast editing of results for use in the clinical context and data export for research.

Please cite this article in press as: Piscicelli C, Pe´rennou D. Visual verticality perception after stroke: A systematic review of methodological approaches and suggestions for standardization. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/ j.rehab.2016.02.004

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Fig. 3. (A) VV orientation and (B) VV uncertainty as a function of different groups of subjects (controls, patients with independent sitting posture [ISP] and without ISP due to contralesional lateropulsion [non-ISP]) and different postural setting (non-maintained body, partially maintained body [trunk maintained upright], maintained body [trunk and head maintained upright]). Data are mean  SEM. Adapted from Piscicelli et al. [58].

The line’s length ranged from < 10 cm [23,30,33,39,41,64] to 90–100 cm [14,57,66]. A recent study of healthy participants showed that this parameter had no effect on VV perception measurement [67]. However, the initial tilt of the line, in terms of side and angle magnitude, affected VV perception assessed with the adjustment method [67]. Most studies did not specify the magnitude of the initial tilt of the line. Among the studies reporting this parameter, the maximum angle of initial tilt ranged from 308 to 608 [4,6,16–19,22,24,30,33–36,39–44,54,55,57–59]. Only one study [48] proposed a protocol of VV assessment with a low magnitude of initial tilt (68). 3.3.3. Type of paradigm Myriad protocols have been used to assess VV perception after stroke (Fig. 4). The paradigms include the hemispheric dome method [2,3,10,12,13,15,17,20,21,50,52,53,60,61] (Fig. 4a), whereby patients look into a hemispheric dome with a surface of 60 cm in

diameter that extends over the entire visual field and is covered with a random pattern of colored dots, providing no cues to gravitational orientation. A linear target is fixed on the shaft of a servomotor. The dome and the target may be rotated. A computer is used to record the difference between the adjusted orientation and the true vertical. In the bucket test [62,63] (Fig. 4b), patients estimate the vertical orientation by attempting to properly align a straight line visible on the bottom of a bucket that is rotated at random by the examiner. The computerized Visual-Spatial Perception Program [29,32,41,45,46,57] offers detailed analysis of visual-spatial perception [68]: the VV measurement consists of vertically orienting an oblique white line presented on a dark background. The visuo-haptic vertical protocol [34–36,40, 54,55,59] (Fig. 4c) consists of manually orienting a metal rod with 10 red diodes fixed on a metal disk and placed before a vertical black panel. A potentiometer displays the angle between the true vertical and the perceived vertical. The rod and frame test

Fig. 4. Different types of paradigms to assess the VV after stroke. a: hemispheric dome method [62]; b: bucket test [62]; c: visuo-haptic vertical [34–36,40,54,55,59]; d: rod and frame test [72]; e–g: homemade protocols with a luminous line presented, either on a computer screen; e [8,18,19,44,58] and f [48] or g: projected on a wall by a video projector [7].

Please cite this article in press as: Piscicelli C, Pe´rennou D. Visual verticality perception after stroke: A systematic review of methodological approaches and suggestions for standardization. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/ j.rehab.2016.02.004

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[38] (Fig. 4d) requires vertically orienting a luminous line with a distractor visual background, static or dynamic, to test the effect of visual cues on VV perception. Finally, various homemade protocols have been used with a mechanical luminescent rod [4] or a luminous line projected on a wall by use of a videoprojector or presented on a computer screen [5–8,18,19,22–24,30,33,37,39,42– 44,48,49,51,56,58,64–66] (Fig. 4e,f). Only Zwergal et al. [62] analyzed the diagnostic validity of various methods by comparing the bucket test and the hemispheric dome method. The authors found no difference in VV values with the methods, with high concordance (r = 0.89). 3.3.4. The task Except for in one study [47], VV perception was always assessed by asking patients to adjust the visual stimulus to the vertical. This procedure may be assimilated to the method of adjustment: the patient is asked to control and adjust the orientation of a stimulus (the luminous line) until it feels vertical. Only Paci et al. [47] assessed VV with a ‘‘two-alternative forced choice’’ procedure requiring patients to report between 2 alternative stimuli briefly presented, the stimulus tilted clockwise or counter-clockwise. These 2 procedures seemed to give comparable results [67]. However, the method to adjust the stimulus was not consistent among studies and might affect the measure. 3.3.5. Response modality Two main types of response modality could be identified. Patients performed the adjustment task by giving the operator verbal instructions on how to adjust the stimulus to the vertical [6–8,17– 19,32,33,39,41–46,48,55–59,62]. An alternative was asking patients to manipulate the stimulus with a joystick [5,15,30,61], a remote control as a potentiometer or a knob [2–4,10,12–14,16,22, 24,27,31,37,51,60,66], a computer mouse [23,64], by rotating the bucket in the bucket test [63] or by rotating the luminous rod in the visuo-haptic vertical task [34–36,40,54]. The effect of the response modality on VV measures was not investigated. Some authors argued that the verbal modality allowed for circumventing possible biases due to handedness, apraxia, learning or executive dysfunctions in stroke patients. The verbal modality did not preclude testing aphasic patients, because a code answer could easily be set up for these patients. The assessment of stroke patients, presenting a set of various deficits, should take into account these characteristics and should adapt to their capacities, especially their cognitive capacities. In the same way, another important issue is the assessment duration, which can be adapted to attentional resources of stroke patients. 3.3.6. Number of trials The number of trials should be preferably even, counterbalancing the leftward and rightward initial tilt in order to reduce the effect of the starting position of the line on VV estimates [67]. Few studies assessed VV with an odd number of trials [20,50,63,65]. We found few justifications for the number of adjustments used to assess VV, although 10 was used in about half of the studies (n = 27/61) [2,3,5,8,10,12–14,19,27,29,32–34,39,42–46,57,58,60– 62,66]. A lower number of 6 trials was less frequently used (n = 12/61 studies) [4,28,30,31,35–37,40,41,49,51,54]. The question of the number of trials required to reach consistency in VV measure was recently addressed by Piscicelli et al. [18]; 10 trials was required to adequately measure VV orientation in nonselected subacute hemispheric stroke patients. However, for complex protocols imposing a decrease in the number of trials for each condition, 6 trials may be sufficient to identify VV biases in 96% of patients. Some studies assessed VV perception in stroke patients with > 10 trials [17,22,24,56,59]. In our opinion, because of a high

fatigability and limited attentional resources of these patients, a too high number of trials might alter the results at the acute or subacute phases after the stroke. A few studies used an extreme number of trials: the minimum being from 2 [16] and the maximum 30 [56]. 3.4. Type of outcome measure VV perception was mainly estimated by the orientation criterion, which reflects the direction perceived as vertical by individuals. This criterion, also called bias or constant error [29,32,45,46,57], is usually calculated by averaging results (deviations from gravitational vertical of the VV perceived) from the number trials performed by the patient [3–5,8,10,12, 13,16,18,19,22–24,33–36,39–44,54,58–60,62–66]. Some authors calculated the mean absolute error [6,7,28,37,49,51,61]. This unsigned mean error in alignment to the vertical was also reported by some authors as an estimation of the uncertainty criterion [48,49], which reflects the robustness of the internal representation of verticality, enhanced by the congruency of somaesthetic and vestibular graviceptive signals [44,58] and the awareness of body orientation [69]. It is a secondary criterion, little reported in the literature [6,7,16,19,22,44,58], and contrary to the orientation criterion, no agreement exists about the best way of estimating the uncertainty in the perception of verticality. When considered, this criterion is mainly expressed as the standard deviation of the mean error [6,7,19,22,44,58]. However, uncertainty was sometimes calculated by the maximum difference between the counter-clockwise and clockwise adjustments [16,37] or the absolute mean error [48,49]. Also, the Visual-Spatial Perception Program determined an interval of uncertainty, thereby indicating the complete range during which the subject considers the displayed line as exactly vertical within each trial. From this value the uncertainty criterion, named ‘‘the difference threshold’’ was calculated as one-half of the interval of uncertainty [29,32,45,57]. 3.5. Ranges of normality Despite the variability in protocols, the ranges of normality only slightly differed between studies. For VV orientation criterion, VV perception was usually considered normal with orientation values of 2.58 to 2.58 [3,8,12,15,17–21,42,44,50,52,53,58] according to robust normal ranges validated congruently with 110 healthy participants aged 20 to > 60 years, with 10 subjects for the decade 10–20 years, with the hemispheric dome method [13] and 33 healthy participants (mean age: 48.8  10.8 years) with a computerized VV perception task [8]. In some studies, the cutoff was 28 [4,12,27,57,66] according to Dichgans et al. [70] or 38 [5–7,16,37,65]. Some other studies used other ranges of normality [28,31,40,59,63,64] adapted to the protocol used. For VV uncertainty criterion, 2 studies used a cutoff of 88 obtained with a sample of 20 healthy participants [5,16], whereas others used a cutoff of 38 validated with 40 healthy subjects [6,7]. VV orientation does not seem to be affected by normal aging, whereas VV uncertainty increases with age [67]. 3.6. Psychometric properties Our knowledge of the psychometric properties of VV assessment is limited. Zwergal et al. [62] investigated the diagnostic validity of their protocol, the bucket test. Comparative measurements showed no difference in the distribution of VV estimates with the hemispheric dome or bucket test, with reliability 90%. Convergent validity has little been investigated. Concordance between VV and haptic vertical perceptions was shown in right brain-damaged patients with neglect [32,55] but not in nonselected hemispheric stroke patients [59]. However, in this latter

Please cite this article in press as: Piscicelli C, Pe´rennou D. Visual verticality perception after stroke: A systematic review of methodological approaches and suggestions for standardization. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/ j.rehab.2016.02.004

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Fig. 5. (A) Intra-rater and (B) inter-rater reliability of the VV orientation assessed with 20 patients with subacute hemispheric stroke. Data are mean  SEM. ICC: intraclass correlation coefficient Adapted from Piscicelli et al. [19].

study, Rousseaux et al. [59] showed a concordance between VV and visuo-haptic vertical tilt with common brain structures involved. Pe´rennou et al. [8] also showed a correlation between VV and postural vertical perception, with many cases of dissociations between these 2 modalities underpinned by common but also specific brain structures. In investigating whether VV measurements are reliable to support wide clinical use, Piscicelli et al. [19] examined for the first time the inter- and intra-rater reliability of VV in hemispheric stroke patients. VV was assessed on 10 trials by asking patients, seated with their trunk and head maintained upright, to verbally adjust a luminous line presented on a computer [8,18,44,58]. This study showed that VV orientation is a reliable measure for subacute hemispheric stroke patients and has excellent inter- and intra-rater reliability (intraclass correlation coefficients > 0.98) (Fig. 5). In addition, the minimal detectable change (MDC) was calculated to examine the variability in the score caused by random measurement error between repeated measurements for an individual. Both clinicians and researchers can use the MDC as a threshold to determine whether the change in score for a patient shows a real improvement (or deterioration) or is due to random measurement error. This threshold can be used to interpret VV evolution after stroke in order to interpret a difference between several measures as resulting from a clinical change (recovery) or possibly as a measurement error. Previous findings suggested a tendency toward recovery of normal VV within weeks or months for most hemispheric stroke patients [3,37]. An MDC < 28 was found, which suggests that a change of  28 can be interpreted as a real change with 95%

confidence in subacute hemispheric stroke patients. This threshold is critical for clinical rehabilitation settings in the follow-up of stroke patients with a tilted perception of verticality but also for clinical stroke trials to study the responsiveness to a specific rehabilitation program. One further step in assessing the psychometric properties of VV perception would be to determine the clinical significance of a change of  28 in clinical practice. For VV uncertainty, our results revealed less satisfactory reliability, especially for inter-rater reliability. In this study, the 2 examiners had different degrees of expertise in VV assessment (novice vs expert), which simulates more closely the assessment conditions of clinical practice or clinical trials in which measurements are frequently taken by different clinicians with different levels of training. This choice might explain the low inter-rater reliability for VV uncertainty. Regarding responsiveness, few data are available. For brainstem stroke, Dieterich and Brandt [2] investigated the time course of recovery and showed that spontaneous reduction in VV tilt occurred over periods from weeks to months, with the most marked improvements occurring exponentially within the first 4 weeks. Interestingly, the time course of lateropulsion was approximately similar. For hemispheric lesions, only Bonan et al. [37] investigated the evolution of VV tilt after stroke. In this study, 60% of the 30 patients with recent stroke had an initial VV tilt as did 39% of these recovering during the first 3 months after stroke. The evolution of VV tilt depended on the side of the lesion, with better recovery in left brain-damaged patients. This poorer recovery of vertical perception after right-side stroke might be involved in the poor recovery of balance after stroke in right brain-damaged patients.

Please cite this article in press as: Piscicelli C, Pe´rennou D. Visual verticality perception after stroke: A systematic review of methodological approaches and suggestions for standardization. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/ j.rehab.2016.02.004

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The predictive validity of VV on postural and gait recovery after stroke remains to be investigated, although some studies tested the relationship between VV and gait and postural disorders [2,6–8]. Dieterich and Brandt [2] interpreted the lateropulsion in patients with Wallenberg’s syndrome after a brainstem stroke as a postural consequence of an abnormal tilt of the internal representation of orientation in space assessed by the VV. For hemispheric stroke, Bonan et al. [7] showed that initial alteration in verticality perception (within 3 months after stroke) was related to a poor score for balance, assessed by the Postural Assessment Scale for Stroke (PASS) [71], at 6 months after stroke. This relationship seemed to be independent of motricity and neglect. However, for a series of 80 hemisphere stroke patients, the correlation between VV estimates and degree of lateropulsion, assessed by the Scale for Contraversive Pushing [33], was weak (r = 0.33) [8]. Tilt of the postural vertical was more closely related to postural disorders than was VV tilt [8].

measure [67] and to obtain reliable VV orientation in subacute stroke patients [18]. Under these conditions, the orientation of the VV is a highly reliable criterion that may be used both in research and routine clinical practice [19]. The consensual values to consider VV orientation as normal are between 2.58 and 2.58 and for VV uncertainty  38. The threshold of  28 can be used to interpret changes in VV perception between repeated measurements for clinical rehabilitation settings in the follow-up of stroke patients with a tilted perception of verticality but also for clinical stroke trials to analyze the responsiveness to a specific rehabilitation program. Indeed, clinical trials are probably the future step in the study of VV perception after stroke. A rigorous and standardized measurement of VV perception should guide the emergence of rehabilitation programs specifically dedicated to the sense of verticality after stroke.

4. Discussion

VV is increasingly being assessed after stroke and appears to be a valid assessment tool. This review provides ways to standardize protocols in order to limit measurement errors and better interpret the results.

This first systematic review of the methodological approaches of visual verticality perception after stroke aimed to synthesize knowledge to help clinicians and researchers establish guidelines for a rigorous and more homogeneous use of this measure in clinical practice and research. This review leads to some recommendations about the patient setting, instructions, and handling and also suggests that training may benefit examiners. The review involved 61 studies assessing VV perception after stroke and reporting data for 1982 patients, tested after hemispheric (70.5%), brainstem (29.5%) or cerebellar (13.1%) stroke. This number of studies reflects the growing interest in this topic, especially in the last 20 years. Because of the varied study designs, patient characteristics, paradigms for VV assessment, settings and reported outcome measures, we focused on a qualitative synthesis of the data collected. This finding is direct evidence of the heterogeneity of the VV assessment methods and argues for a standardization of some aspects of VV measurements. Most if not all of the testing procedures may be easily implemented for routine clinical use; several have the CE marking and are commercialized. However, the psychometric properties of VV assessment must be further analyzed, taking into account the types of paradigms and task. In light of this analysis, we recommend the electronic assessment procedure, whose direct and automatic recording of data circumvents measurement bias due to operator intervention. This assessment involves masking the edges of the computer screen; maintaining the trunk upright for validity of results of VV orientation is the test’s main criterion, if not the only criterion for clinical practice. This maintenance of an upright body is mostly achieved by using a chinrest with an adjustable height [2,3,5–7,10,12–15,17,20– 22,24,29,32,45–47,50,52,53,55,57,60,61,65,66]. This setting is assumed to be sufficient to control the orientation of the trunk because supporting the head maintains the trunk upright. However, an additional valid result for VV uncertainty requires maintaining the head upright with a suitable device because a chinrest maintains the trunk upright and controls the head position on the vertical axis but does not preclude any head rotation in roll. Measuring VV without any body maintenance is valid for only subjects with satisfactory balance abilities. The verbal modality response seems to be a good way to assess stroke patients who may have motor disorders resulting in problems related to handedness and cognitive disorders such apraxia, learning or executive dysfunctions compromising the learning and the use of a response device. A verbal code answer can easily be set up for aphasic patients. Moreover, VV perception should be assessed with an even number of trials, between 6 and 10, to account for the effect of the starting position of the line on the VV

5. Conclusion

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Please cite this article in press as: Piscicelli C, Pe´rennou D. Visual verticality perception after stroke: A systematic review of methodological approaches and suggestions for standardization. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/ j.rehab.2016.02.004