Molina 2019
Molina 2019
DOI:10.3233/NRE-182642
IOS Press
Abstract.
BACKGROUND: The interpretation of the verticality of the environment is crucial for a proper body balance. The subjective
visual vertical test (SVV) is a widely used method to determine the visual perception of the verticality, whose alteration has
been related with poor functional status.
OBJECTIVE: To analyze the visual perception of the verticality in neurological patients in comparison with healthy controls.
METHODS: We searched PubMed, Scopus, and Scielo from the start of the databases until October 2017 and manually
searched the reference lists of studies comparing SVV values between neurological patients and controls. Standardized mean
difference (SMD) and subgroup analysis were used to analyze differences between neurological patients and healthy subjects
and between stroke and non-stroke patients, respectively.
RESULTS: A total of 1,916 subjects from 31 studies were included. Neurological patients misestimate the true vertical
in comparison with controls (SMD = 1.05; 95% CI: 0.81, 1.28). The misperception of the verticality was higher in stroke
patients (SMD = 1.35; 95% CI: 1.02, 1.68) than in patients with other neurological conditions (SMD = 0.48; 95% CI: 0.29,
0.68).
CONCLUSIONS: Neurological patients showed a misperception of the verticality, estimated using the SVV. The neurological
pathology that most alters the SVV is stroke.
Keywords: Stroke, neurological disorders, gravity perception, subjective visual vertical, balance
ISSN 1053-8135/19/$35.00 © 2019 – IOS Press and the authors. All rights reserved
380 F. Molina et al. / Misperception of the subjective visual vertical in neurological patients with or without stroke
sion (weeks from the damage), protocol for SVV inconsistency (I2 ) of Higgins et al., 2011. Publication
measurement (SVV Upstanding/SVV Sitting/Rod bias was assessed by the funnel plot, and the pooled
and Frame), presence/absence of hemispatial neglect, effect was estimated (taking into account any possible
and presence/absence of stroke. Disagreements publication bias) by the Trim and Fill method (Duval
between reviewers were solved by consensus. The & Tweedie, 2000). Sensitivity analyses were con-
pooled effect was calculated as standardized mean ducted to assess the contribution of the studies to the
difference (SMD). pooled estimate in the meta-analysis (leave-one-out
method) (Cooper et al., 2009). The Newcastle-Ottawa
2.4. Analyses Scale (NOS) was used to assess the quality of the
Analyses were performed using the Com- studies included in the meta-analysis.
prehensive Meta-analysis 3.3.070. Following the
recommendations of Cooper et al., 2009, the random- 3. Results
effects model was used for estimating the pooled
effects and their 95% confidence interval (CI) to The 31 studies included in the present meta-
improve the generalization of the study findings to analysis were comprised of 54 samples with 54
any exposed or non-exposed subject. The Q test independent comparisons. The study selection pro-
was used for performing the heterogeneity analysis, cess is summarized in the PRISMA flow chart
which was completed by calculating the degree of (Fig. 1). The total number of participants was 1,916
Table 1
Characteristics of the studies included in the meta-analysis
Samples N Location Vascular Stroke
Anastasopoulus et al. 1999 1 38 Mixed Yes Yes
Asai et al. 2009 1 33 Brain Yes No
Barnett-Cowan et al. 2010 2 44 Brain No No
Barra et al. 2010 1 50 Brain Yes Yes
Blomsterwall et al. 2011 1 26 Brain No No
Bonan et al. 2006a 2 70 Brain Yes Yes
Bonan et al. 2006b 1 53 Brain Yes Yes
Bonan et al. 2007 1 48 Brain Yes Yes
Braem et al. 2014 2 32 Brain Yes Yes
Chandrakumar et al. 2010 1 35 Mixed Yes Yes
Crevits et al. 2007 1 47 Brain Yes No
Crevits et al. 2012 1 143 Brain Yes No
Frisen et al. 2010 4 201 Brain No No
Funk et al. 2010 3 48 Brain Yes Yes
Funk et al. 2011 3 72 Brain Yes Yes
Ishikura et al. 1999 1 28 Brain Yes Yes
Johannsen et al. 2006 2 35 Brain Yes Yes
Khattab et al. 2012 1 94 Brain No No
Mansfield et al. 2015 2 34 Mixed Yes Yes
Pereira et al. 2014 1 90 Brain No No
Pérennou et al. 2008 4 275 Brain / Mixed Yes Yes
Pinar et al. 2005 1 33 Brain Yes No
Saj et al. 2005 3 34 Brain Yes Yes
Saj et al. 2006 2 28 Brain Yes Yes
Saj et al. 2012 4 89 Brain Yes Yes
Scocco et al. 2014 1 27 Brain No No
Snowdown et al. 2005 1 21 Brain Yes Yes
Tarnutzer et al. 2008 1 20 Brain No No
Tarnutzer et al. 2011 1 22 Mixed No No
Utz et al. 2011 2 66 Brain Yes Yes
Yelnik et al. 2002 2 80 Brain Yes Yes
Abbreviations: N: sample size; Mixed: Several regions of the Central Nervous System.
(mean per sample: 35.5). Table 1 summarizes the (Anastasopoulos, Bronstein, Haslwanter, Fetter, &
main characteristics of the studies. In 48 of the 54 Dichgans, 1999; Chandrakumar, Blakeman, Goltz,
samples, the neurological lesions were located in the Sharpe, & Wong, 2011; Mansfield, et al., 2015; Peren-
brain (Asai, et al., 2009; Barnet-Cowan, et al., 2010; nou, et al., 2008; Tarnutzer, Shaikh, Palla, Straumann,
Barra, et al., 2010; Blomsterwall, Frisén, & Wikkelso, & Marti, 2011), included mixed lesions (brain and
2011; Bonan, Derighetti, Guellez-Leman, BradaÏ, & brainstem-medulla). Concerning the origin of the
Yelnik, 2006; Bonan, Guettard, Leman, Colle, & lesions, vascular injuries were analyzed in 42 sam-
Yelnik, 2006; Bonan, et al., 2007; Braem, Honore, ples (Asai et al., 2009; Barra et al., 2010; Bonan et al.,
Rousseaux, Saj, & Coello, 2014; Crevits, Vanacker, 2006; Bonan et al., 2006; Bonan et al., 2007; Braem
& Verraes, 2012; Crevits, Venhovens, Vanoutrive, et al., 2014; Crevits et al., 2012; Crevits et al., 2007;
& Debruyne, 2007; Frisén, 2010; Funk, Finke, Funk et al., 2011; Funk et al., 2010; Ishikura, 1999;
Muller, Utz, & Kerkhoff, 2011; Funk, Finke, Muller, Johannsen et al., 2006; Pinar et al., 2005; Saj et al.,
Utz, & Kerkhoff, 2010; Ishikura, 1999; Johannsen, 2012; Saj et al., 2005; Saj et al., (2006); Snowdon
Fruhmann-Berger, & Karnath, 2006; Khattab, et al., & Scott, 2005; Utz et al., 2011; Yelnik et al., 2002;
2012; Pereira, Kanashiro, Maia, & Barbosa, 2014; Anastosopoulos et al., 1999; Chandrakumar et al.,
Pinar, Ardic, Topuz, & Kara, 2005; Saj, Honore, 2011; Mansfield et al., 2015; Perennou et al., 2008).
Bernati, & Rousseaux, 2012; Saj, Honore, Coello, The most common neurological disorder was stroke
& Rousseaux, 2005; Saj, Honore, & Rousseaux, (38 samples) (Barra et al., 2010; Bonan et al., 2006;
2006; Scocco, Wagner, Racosta, Chade, & Gershanik, Bonan et al., 2006; Bonan et al., 2007; Braem et al.,
2014; Snowdon & Scott, 2005; Tarnutzer, Marti, & 2014; Funk et al., 2011; Funk et al., 2010; Ishikura,
Straumann, 2008; Utz, et al., 2011; Yelnik, et al., 1999; Johannsen et al., 2006; Saj et al., 2012; Saj
2002). The other 6 samples, obtained from 5 studies et al., 2005; Saj et al., (2006); Snowdon & Scott, 2005;
F. Molina et al. / Misperception of the subjective visual vertical in neurological patients with or without stroke 383
Fig. 2. Forest plot for subjective visual vertical deviation from the true vertical (effect sizes are expressed as standardized mean difference).
cues play a critical role in determining the vertical- Our main finding is that patients with neurologi-
ity of the environment and of the subject. The SVV cal diseases misestimated the SVV in comparison to
test is widely used to estimate the visual perception healthy subjects. Such deviation from the true vertical
of verticality in neurological patients. However, the in neurological patients suggests that neural damage
scientific literature shows controversial results on the may cause a visual deficient interpretation of the ver-
perception of the verticality in these patients. ticality, leading to a misalignment of the head and
F. Molina et al. / Misperception of the subjective visual vertical in neurological patients with or without stroke 385
Fig. 4. Scatterplots.
Fig. 6. Funnel Plot of the “non-stroke” subgroup.
of the body axis (Perennou et al., 2008; Barra, et al.,
2008). This abnormal body position may trigger sev- perception of the verticality to improve their balance
eral additional symptoms and co-morbidities as a (Cohen, 2013).
higher risk of falling (de Groot, et al., 2014). Along Our data also showed that stroke patients mis-
this line, recent studies have reported that the SVV perceived the SVV to a greater extent than patients
deviation detected in subjects with multiple sclero- suffering from other neurological disorders, suggest-
sis (da Fonseca et al., 2016) and Parkinson’s disease ing that stroke patients may be at higher risk of falls
(Pereira et al., 2014) is correlated with a higher risk (Cho & Lee, 2013) than patients with other neuro-
of falling. logical pathologies due to a greater misperception of
As stated above, the sense of verticality is the result the verticality (Baggio, et al., 2016). However, fur-
of the function of several CNS areas distributed over ther research is needed to confirm this hypothesis
the brainstem, brain and cerebellum, among others. before proposing the determination of the SVV as
Consequently, an injury in one or more of these areas a predictor of the risk of falling in stroke patients.
may alter the perception of the verticality. Our results The differences found in the SVV estimation between
have shown that all the neurological patients failed stroke and non-stroke patients may be explained by
to estimate the SVV in comparison with the healthy considering the temporary phase of the neurologi-
controls and that the most frequently damaged area in cal damage. The majority of stroke patients were
these patients was the brain, supporting the hypoth- recruited during the acute or sub-acute phase of the
esis that any CNS damage may alter the perception disease (<6 months) in most of the studies included
of the verticality. Therefore, patients with any neu- in the present review. In contrast, the non-stroke
rological condition should be retrained in the visual patients suffered from chronic neurological condi-
386 F. Molina et al. / Misperception of the subjective visual vertical in neurological patients with or without stroke
Table 3
Subgroup analysis
k N Point Lower Upper I2 Egger Trim and
estimate Limit Limit test Fill
(SMD) (p value) (% of variation)
“Stroke” subgroup 38 1136 1.35 1.02 1.68 33.7 % 0.0007 7.4 %
“Non-stroke” subgroup 16 780 0.48 0.29 0.68 10.4 % 0.39 6.3 %
Abbreviations: k: number of studies; N: total sample size; SMD: Standardised Mean Difference.
tions (hydrocephalus, multiple sclerosis, Parkinson’s on the visual perception of the verticality (Lucertini
disease, migraine), i.e., with a longer time of dis- et al., 2011).
ease progression. In this sense, it is well established The present systematic review and meta-analysis
that the CNS may mitigate the severity of the initial has some limitations. Some of the studies found dur-
symptoms of a neural injury due to the neuroplasticity ing the searching process were not included in this
phenomena. Thus, adaptive or compensatory mech- meta-analysis for not expressing the SVV data of the
anisms have been widely described in patients with control group in numerical values. On the other hand,
vestibular disorders (Hubner, Khan, & Migliaccio, the disease features were not always available, which
2017; Martin-Saez, et al., 2017). Stroke also triggers limited the scope of the findings of this review. More-
the neuroplasticity process, improving the SVV esti- over, there was great variability in the protocols used
mation at 3 months from the lesion (Lucertini, De by the selected studies for determining the SVV. For
Angelis, Martelli, Zolesi, & Tomao, 2011). However, future research, we recommend a standardization of
meta-regression using the moderating variable “time the SVV protocol following the recommendations
of progression” did not explain a significant percent- of Piscicelli et al., 2016, to obtain a reliable tool
age of the variability, probably because only 24 of for determining the misperception of the verticality
the 46 comparisons analyzed indicated the time of in patients with different pathologies. Correlations
disease progression. On the other hand, stroke fre- among the SVV, time of disease progression and risk
quently occurs in the middle cerebral artery area and of falling should be investigated in stroke patients.
may cause acute and focal damage to balance and In summary, this study is the first meta-analysis
eye-control-related brain areas (eg: insula, temporal that investigates the visual perception of the verti-
and parietal lobe, middle frontal gyrus) (Yeo, Jang, & cality in neurological patients. The findings of the
Kwon, 2017), while the other neurological diseases present systematic review evidence that the visual
usually cause diffuse damage. In addition, the major- perception of the verticality, determined using the
ity of the studies analyzed recruited patients with right SVV test, is altered in patients with neurological dis-
hemisphere stroke, which could explain our results eases. The neurological pathology that most alters
since right hemispheric lesions are associated with the SVV is stroke. Although we did not find any
poorer recovery of the verticality perception than left difference when determining the SVV using diverse
hemispheric lesions (Bonan, Leman, Legargasson, experimental procedures, a standardized protocol
Guichard, & Yelnik, 2006). should be established and used in future research to
Our results did not show any effect of the type simplify the comparison of the results from different
of protocol used for determining the SVV, suggest- studies. The time of progression of neurological dis-
ing that there are no difference when estimating the eases should also be considered in future studies to
SVV in an upright position versus a sitting position. determine the real effect of the neuroplasticity pro-
This is an interesting result because it contradicts cess on the recovery/retrain of the visual perception
the hypothesis of some researchers that lower limb of the verticality. Further research is needed to con-
proprioception may be decisive in determining the firm the effectiveness of the SVV determination as a
verticality perception of body and head (Barbieri, prognosis method for recovery and risk of falling in
et al., 2008; Vaugoyeau, Hakam, & Azulay, 2011) stroke patients.
and, consequently, the visual perception of the verti-
cality. However, our results suggest that lower limb
proprioceptive information does not influence the Conflict of interest
verticality perception. In agree with our results, other
authors failed to find any implication of body posture The authors declare no conflict of interest.
F. Molina et al. / Misperception of the subjective visual vertical in neurological patients with or without stroke 387
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