Introduction
Methods
Search strategy
Study selection
Data extraction and validation
Results
Included studies
Definition
Author and year [references] | Visual responsea | Descriptions (quotes from original text) |
---|---|---|
Andrews 1996, report of International Working Party on the Management on PVS [26] | Visual tracking | “Eye tracking is when a patient follows a moving object by moving the eyes” |
Andrews 1996, summary of report International working Party Management on PVS [25] | Visual tracking | “Tracking eye movements following objects or people” |
Ansell et al. 1989 [32] | Eye tracking | “Eye tracking: localizing to a visual stimulus” |
Horizontal tracking | “Horizontal tracking: ability to follow visually through left and right visual fields” | |
Vertical tracking | “Vertical tracking: ability to follow visually through upper and lower visual fields” | |
Eye contact | “Eye contact: patient’s gaze during the majority (50%) of the session” | |
“Eyes focussed on the examiner (50% or more)” | ||
Giacino et al. 2002 [3] | Pursuit eye movements | “Pursuit eye movements or sustained fixation that occur in direct response to moving or salient stimuli.” |
Sustained fixation | ||
Rader and Ellis 1994 [34] | Visual tracking < 3 s | “Eye movements toward stimulus (patient appears to be “looking at” stimulus and/or stimulator) for less than 3 s.” |
Visual tracking > 3 s | “Eye movements toward stimulus (patient appears to be “looking at” stimulus and/or stimulator) for more than 3 s.” | |
Wade and Johnston 1999 [33] | Visual fixation | “···visual fixation active looking at or for objects” |
Assessment and operationalization of VP and VF
Author and year [references] | Assessment method | Purpose of method | Method of testing | Operationalization |
---|---|---|---|---|
Ansell et al. 1989 [32] | WNSSP | Measuring cognitive and communicative function in severely head injured patients | Present mirror, picture, object in midline position Slowly move item from left to right across midline. Repeat several times, if necessary Use colored pictures, preferentially family pictures. Use bright objects or objects with moving parts Tracking of individual: walk to the opposite side of the patient’s bed Test tracking of all stimuli in horizontal and vertical planes | Scoring system (points) Horizontal tracking: 0: no response 1: following from midline to 1 side 2: following from midline to 2 sides 3: following across midline Vertical tracking: 0: no response 1: following in 1 direction 2 following in 2 directions |
Bender Pape 2011 [35] | DOCS | Measuring neurobehavioral functioning during coma recovery | Present 3D objects, familiar faces picture and mirror Present in left visual field and slowly move across midline to right visual field, and vice versa Present 3D object/familiar face in middle visual field and slowly move upward and downward Present each item as many times as necessary to determine best response Test in horizontal and vertical planes | Scoring system (points) 2: localized response. Visual orientation toward object Separate scores for each visual field. Score 2 if tracking in at least one visual field. If 2 is not scored, have subject track themselves with a mirror Separate scores for each visual field |
Borer et al. 2002 [36] | LCS | Provide information about communicative abilities in minimally responsive patients and indicator of rehabilitation potential | Object, peoplea Vertical and horizontal planes | Scoring system (points): 0: no tracking 1: inconsistent selective tracking 2: consistent selective tracking 3: diminishing tracking 4: constant qualitative tracking |
CRS-R | Diagnostic distinction between UWS/VS and MCS | Mirror, 4-6 inches in front of face, verbally encourage patient to fixate on mirror, move 45° to left, right, up, down Repeat procedure, total of 2 trials in each direction administered |
Response scored if:
Eyes must follow mirror for 45° without loss of fixation on 2 occasions in any direction. | |
CAMMRI | Detection of subtle signs of consciousness | Pictures/photographs, mirror, target stick (circle mounted on a stick). Up to three stimuli can be presented Instruct client to look at stimulus, place 18 inches away from eye, tell client to keep looking at moving target. If no tracking observed with one stimulus, try another stimulus. Horizontal and vertical: slight arc of 45° from midline to left/right and up/down, respectively Diagonal tracking: test only if at least partial horizontal and vertical tracking are observed, move stimulus slowly diagonally. Start in visual quadrant that showed the best tracking Do 3 tests for each plane | Scoring system (points): Fixes gaze: 0: no fixation, 1: fixation Horizontal and Vertical Tracking 0: no tracking, 1: partial tracking in left, right, upper or lower field (1 point for each field)b 2: full tracking in left, right, upper or lower field (2 points for each field)c Diagonal tracking 0: no tracking 1: tracking | |
Rader and Ellis 1994 [34] | SSAM | Measuring the unconscious patient for a long period over time | Separate assessor and rater looking at stimulus or stimulator |
Best response to stimulation recorded, points scored
1: eye movement not different from baseline 2: eye opening in response to stimulus 3: visual tracking < 3 s: Eye movement toward stimulus, patient appears to be “looking at” stimulus or stimulator less than 3 s 4: visual tracking > 3 s: Eye movement toward stimulus, patient appears to be “looking at” stimulus or stimulator more than 3 s 5: blinks, opens, or closes eyes in response to command 6: answer to simple questions by eye movements |
CNC | Detection of small changes in neurobehavioral status in patients in UWS/VS or near-vegetative states | Tell patient “look at me” move your face 20 inches away from side to side Horizontal plane 5 trials |
Scoring system (points)
0: sustained tracking (at least 3x) 2: partial tracking (1–2×) 4: no tracking | |
Stokes et al. 2016 [43] | STAR | Graded assessment of motor, sensory and communicative responses to sensory programme | Mirror Hold a mirror in front of the patient, move to all four quadrants of visual field. Horizontal, vertical Repeat 3 times (4 trials in total), with a ten second delay after each trial. | Sustained visual pursuit showing localization response: Fixates on mirror for at least two seconds, at least twice, during the four trials |
WHIM | Monitoring changes from coma to consciousness |
Behavior observed
Item 12: eyes follow person moving in line of vision |
Operational definition
Eyes move in direction of person, from midline to either left or right | |
Behavior observed
Item 16: turns head to person who is talking |
Operational definition
Moves eyes or turns head at person | |||
Behavior observed
Item 17: watches person moving in line of vision. Person moves from one side to other side of the bed |
Operational definition:
Eyes follow from end of bed to left or right or both. | |||
Behavior observed
Item 18: tracks for 3–5 s. Attract patient’s attention with a brightly colored object, move through the visual field |
Operational definition
If patient tracks through at least 90 degrees |
Author and year [references] | Assessment method | Purpose of method | Method of testing | Operationalization |
---|---|---|---|---|
Ansell et al. 1989 [32] | WNNSP | Measuring cognitive and communicative function in severely head injured patients | Observation of focusing of patient on the examiner | Scoring system (points) 0: eyes closed, 1: eyes open, not focused on the examiner, 2: eyes focused on examiner (50% or more), 9: unable to open the eyes (CN III paralysis) |
Bender Pape 2011 [35] | DOCS | Measuring neurobehavioral functioning during coma recovery | Focus on familiar face. Hold picture of familiar person to patient for at least 1 year prior to injury approximately 18 inches to face for 5–10 s. Test in upper, lower, middle, left and right visual field | Scoring system (points) 2: localized response. Visual orientation toward object. Separate scores for each visual field Score 2 if focusing on familiar face in at least one visual field |
Borer-Alafi et al. 2002 [36] | LCS | Provide information about communicative abilities in minimally responsive patients and indicator of rehabilitation potential | Gaze is observeda | Scoring system (points): 0: no use of the visual channel: closed eyes, no eye movements, no papillary response to stimuli, et cetera 1: congealed, freezed gaze 2: aroused look, eye movements apparently directed to the environment 3: inconsistency in focusing on stimuli 4: aroused look with consistent focus on stimuli |
CRS-R | Diagnostic distinction between UWS/VS and MCS | Brightly colored or illuminated object presented in front of patient’s face, readily move to upper, lower, right, left visual fields Horizontal and vertical plane 2 trials in each plane |
Scoring criteria
Eyes move from initial fixation point and re-fixate at least 2 s on new target. At least 2 episodes of fixation are required | |
CAMMRI | Detection of subtle signs of consciousness | Various stimuli: pictures/photographs, mirror, target stick (circle mounted on a stick) Position yourself so that you can present the stimulus in the client’s visual midline Tell client you have something for him to see. Ask him to try and do his best Place target where eye appears to look and 18” away from eye Move target away 6” or more where target was. Observe if the eye(s) look at the target and note for how long (less than 2 s or at least 2 s) Try to use visual targets of interest. Up to three stimuli can be presented. Do 4 tests: up/downward, left/right | Scoring system (points) Score 0: no fixation in any of the 4 trials, discontinue visual response testing (do not test visual tracking) Score 1: If client fixates gaze, score 1 and proceed with visual tracking test | |
CNC | Detection of small changes in neurobehavioral status in patients in UWS/VS or near-vegetative states | Light flashes 1 per second, in front, slightly left, right up and down, each trial 5 trials |
Scoring system (points)
0: sustained fixation or avoidance (at least 3×) 2: partial fixation (1–2×) 4: none | |
WHIM | Monitoring changes from coma to consciousness |
Behavior observed
Item 5: looks at person briefly |
Operational definition:
Eyes move aimlessly but remain on object/person when noticed. Briefly: impression of looking at | |
Behavior observed
Item 8: makes eye contact. Stand where patient is not directly seeing you, call patient’s name |
Operational definition:
Patient switches gaze and maintains eye contact for at least 3 s | |||
Behavior observed
Item 9: patient is looking to person who is talking to them |
Operational definition
Gaze switch to person who is talking, at least for 3 s | |||
Behavior observed
Item 13: looks at person giving attention |
Operational definition
Eyes rest at least 3 s on person giving attention | |||
Behavior observed
Item 24: maintains eye contact for ≥ 5 s |
Operational definition
Looks at person for 5 s or longer | |||
Behavior observed
tem 28: looks at object when requested, hold brightly colored object out of view, ask patient to look at object |
Operational definition
Holds up brightly colored object out of patients immediate view and ask patient to look at it | |||
Behavior observed
Item 33: seeks eye contact |
Operational definition
Moves head or eyes to make eye contact and maintains this ≥ 3 s | |||
Behavior observed
Item 35: looks at/explores pictures etc. |
Operational definition
Pictures, photographs etc.: looks to, puts down, looks at another picture, etc. | |||
Behavior observed
Item 36: switches gaze from one person to another |
Operational definition
Two people present in room positioned so that patient’s eyes must move or head must be turned to switch gaze from one person to the other. Spontaneously looks from one person to another |
Assessment of visual pursuit
Author, year [references] | Assessment item | Population | Assessment method | Results of study | Conclusion of authors |
---|---|---|---|---|---|
Ansell 1995 [45] | Direction of tracking | Closed head injury (n = 76) | WNSSP | 48% showed preference: 28% preference of tracking in horizontal plane, 20% in vertical plane No significant differences in tracking preference between patients who recovered and those who did not | Individual preferences for plane of tracking, no group effects |
Type of stimulus | WNSSP 4 stimuli Mirror Individual Meaningful picture Object (snow globe) | Mean visual scores (points) Mirror 36.4 Individual 17.0 Picture 21.3 Object 18.7 | Patients who recovered to consciousness had higher visual tracking scores on the WNSSP when a mirror was used | ||
Candelieri et al. 2011 [46] | Time of assessment | UWS/VS (n = 9), MCS (n = 13) | CRS-R | Highest probability of observing visual tracking: 10.30 AM and 3.00 PM, lowest probability of detecting visual tracking: 2.00 PM | Time of assessment influences probability of detecting visual tracking |
Thonnard et al. 2014 [47] | Type of stimulus | MCS (n = 88) | CRS-R | Patients tracked mirror (97%) over person (69%) and object (57%) | Majority of patients showed visual tracking when mirror was used |
Direction of VP | MCS- (n = 47), MCS + (n = 47) | CRS-R | Entire group: significantly more horizontal (n = 80) than vertical tracking (n = 61) MCS-: significantly more horizontal (n = 41) than vertical tracking (n = 35) MCS + : no significant difference between horizontal and vertical tracking. Chronic patients: significantly more horizontal (n = 61) than vertical tracking (n = 47) | Patients in MCS showed preferential horizontal visual pursuit compared to vertical visual pursuit | |
Trojano et al. 2012 [48] | Quantitative assessment | UWS/VS (n = 9), MCS (n = 9) | Infrared eye tracker: Visual pursuit defined as series (bouts) of fixations Images of parrot or circle | On-target fixations: UWS/VS 4.9% (below chance level of 10%) MCS 32.9% | Proportion of on-target fixations significantly differentiated MCS from UWS/VS, whereas mean duration of fixation bouts did not |
Trojano et al. 2013 [49] | Personal relevant stimulus | UWS/VS (n = 13), MCS (n = 13) | Infrared eye tracker Images of parrot or circle or face of relative | MCS: significant higher % of on-target fixations (37.3%) when looking at relative’s face compared to circle (29.9%) and parrot (30.6%) | Higher percentage of tracking to a personal relevant stimulus |
Turner-Stokes et al. 2015 [50] | Person/object | UWS/VS (n = 12) MCS- (n = 12) MCS + (n = 15) Emerged (n = 26) | WHIM |
Observed reaction
state of consciousness
% Eyes follow person moving in line of vision MCS minus VS 1%; MCS- 38%; MCS + : 73% Tracks brightly colored object for 3-5 s: MCS minus VS 1%; MCS- 24%; MCS + 59% Watches person moving in line of vision MCS minus VS 0%; MCS- 27%; MCS + 63% | No conclusiona |
Vanhaudenhuyse et al. 2008 [51] | Type of stimulus | MCS (n = 51) | CRS-R | Detection of visual tracking in individuals who showed visual tracking: mirror 95%, person 66% and object 55%, only tracking mirror 29% | More than a fifth of the patients only tracked a mirror (and not a moving person or object) |
Assessment of visual fixation
Author, year [references] | Assessment item | Population | Assessment method | Results | Conclusion of authors |
---|---|---|---|---|---|
Di et al. 2014 [52] | Use of mirror and/or ball and/or light | UWS/VS (n = 43) MCS (n = 38) | CRS-R | 49% of total population showed VF (all MCS); 48% showed VF in response to mirror, 28% to ball, 25% to light | The frequency of VF in patients with DOC is related to the stimulus used. MCS patients tended to fixate significantly more on their own reflection compared to a brightly colored or illuminated object. |
Pan et al. 2014 [53] | Subject’s own facial photo and an unfamiliar photo | Healthy Subjects (n = 4) UWS/VS (n = 4) MCS (n = 3) LIS (n = 1) | Visual hybrid brain computer interface CRS-R | Run 1: looking at own photo, accuracies in 5/8 patients (2 UWS/VS, 2 MCS, 1 LIS) Run 2: looking at unfamiliar photos, accuracies in 3/5 patients (1 UWS/VS, 1 MCS, 1 LIS) Run 3: looking at either own photo or unfamiliar photos, accuracies in 3/5 patients (1 UWS/VS, 1 MCS, 1 LIS), indicative of command following | Use of P300 and SSVEP BCI showed that VS, MCS and LIS patients looked accurately at either familiar or unfamiliar photos or to both photos. |
Turner-Stokes et al. 2015 [50] | Fixation at individual or object | UWS/VS (n = 12) MCS- (n = 12) MCS + (n = 15) Emerged (n = 26) | WHIM item-by-item analysis |
Observed reaction
State of consciousness
% Looks at person briefly UWS/VS UWS/VS: 14%; MCS-: 65%; MCS + 94% Makes eye contact (briefly) UWS/VS UWS/VS: 5%; MCS-: 35%; MCS + : 76% Looks at person giving attention UWS/VS UWS/VS 1%; MCS-: 36%; MCS + : 74% Looks at person talking to them (at least 3 s) UWS/VS UWS/VS: 1% MCS-: 32%; MCS + : 71% Maintains eye contact for 5 s and more: UWS/VS UWS/VS: 3%; MCS-: 28%; MCS + : 59% Looks at object when requested MCS minus UWS/VS: 0%; MCS-: 15%; MCS + 42% Seeks eye contact: MCS minus UWS/VS: 0%, MCS-: 6%; MCS + 37% Looks at and apparently explores pictures MCS minus UWS/VS: 0%; MCS-: 1%; MCS + : 27% Switches gaze spontaneously from one person to another MCS minus UWS/VS: 0%, MCS-: 1%; MCS + : 22% | No conclusion about VFa |
Whyte and DiPasquale, 1995 [54] | Photos of patient’s family and plain white card | Minimally responsive patients (n = 6) | Photo and card presented in left/right visual field | Diagnosis on vision and visual attention Normal vision in both fields, monocular lesion, homonymous hemianopia left, homonymous hemianopia + possible impairment right eye, left sided extinction, right sided visual inattention | Single subject experimental protocols can be useful to assess vision and visual attention in minimally responsive patients since validated assessment methods are lacking |
Zhu et al. 2009 [55] | Intimate family photos and pictures with emotional content from IAPS database | MCS (n = 9) Healthy controls (n = 10) | Family pictures, high- and medium stimulating pictures fMRI | Family pictures: 6/9 MCS patients show widespread activation in visual network, activation volume lower than in healthy subjects, but activation in network was similar High stimulating pictures: 2/9 MCS patients activation in visual network. Medium stimulating pictures 1/9 MCS patient activation in visual network | Pictures of family members with emotional valence, with which MCS patients were very familiar prior to their loss of consciousness, elicit greater activation of visual activity in the associated visual network |
Influencing factors
Author, year [References] | Factors | Population | Assessment method | Results of authors | Conclusion of authors |
---|---|---|---|---|---|
Andrews et al. 1996 [6] | Visual impairment/blindness | UWS/VS (n = 40) admitted 1992–1995 | Diagnosis derived from medical records | 17/40 (43%) were misdiagnosed, 11/17 (65%) were blind or severely visually impaired | The very high prevalence of visual impairment is a complicating factor since physicians making a diagnosis of the vegetative state place great emphasis on the inability to visually track or blink to threat |
Chatelle et al. 2016 [61] | Oculomotor defects | DOC (n = 1190); UWS/VS (n = 464) MCS (n = 586) | CRS-R | Oculomotor factors and improbable CRS-R scoresa Ptosis or eye lid apraxia: VF/unarousable Bilateral optic nerve damage, Terson syndrome, cortical blindness: No visual response/consistent command following No visual response/functional communication Third and fourth cranial nerve palsy, ocular apraxia, visual agnosia: VF/functional communication VP/functional communication | CRS-R scores are subject to attributable inaccuracy of examiner error and other confounding that can lead to misinterpretation of results |
Cortese et al. 2015 [56] | Variation during the day | UWS/VS (n = 7) MCS (n = 12) | CRS-R | CRS-R visual subscale higher in the morning than in the afternoon | CRS-R differences between morning and afternoon are likely to reflect individual changes in patient’s visual, auditory and motor conceivably due to changes in neuronal/non neuronal factors that modulate the brain state |
Estraneo et al. 2015 [57] | Profession and experience of assessors | DOC (n = 27) | CRS-R | IRR CRS-R visual subscale All raters k = 0.73 Physicians k = 0.81 Psychologists k = 0.68 Nurse/physiotherapist/speech therapist k = 0.73 Expertise high (> 24 months) k = 0.81 medium (12-24 months) k = 0.62 low (< 12 months) k = 0.68 | Results did not change as a function of professional specialities or experience Good IRR was found for all subscales, especially for the visual subscale |
Estraneo et al. 2015 [62] | Oculomotor defects | MCS (n = 52) | CRS-R | 9/52 MCS patients could not produce non-reflexive movements in the visual subscale | The visual subscale of he CRS-R could misdiagnose as UWS/VS as MCS patients with oculomotor defects could not produce non-reflexive responses on the visual subscale |
Godbolt et al., 2012 [6] | Duration of assessment | DOC (n = 10) | CRS-R SMART | In 4/10 differences in diagnosis between CRS-R (2 assessments of 50 min) and SMART (10 assessments of 60 min). 2 additional MCS diagnosis based on visual fixation and visual tracking | Brief behavioural assessment is not as effective as extended assessment in detecting non-vegetative behaviours. Total time spent in behavioural assessment is likely important |
Lovstad et al. 2010 [58] | Experience of assessors | DOC (n = 31) | CRS-R | IRR experienced raters k = 0.46 IRR l less experienced raters k = 0.47 TRR experienced raters k = 0.86 TRR less experienced raters k = 0.57 | The auditory and visual subscales might be most susceptible to interrater disagreement for less experienced raters. |
Sattin et al. 2014 [59] | Presence of informal caregiver | DOC (n = 153) UWS/VS 53% MCS 40% | CRS-R | Significant difference in visual subscale between CRS-R done by rater alone and CRS-R done by rater + informal caregiver (effect size Cohen’s D 0.33). Visual subscale scores were higher in assessments of rater + informal caregiver in MCS and severe disability compared to UWS/VS | Informal caregivers can increase capacity of raters to detect visual responses Visual stimuli furnished by familiar persons could be more attractive |