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. 2021 Apr 15;16(4):e0249467. doi: 10.1371/journal.pone.0249467

Changes in plantar load distribution in legally blind subjects

Ketlin Jaquelline Santana Castro 1, Railson Cruz Salomão 2, Newton Quintino Feitosa Jr 2, Leonardo Dutra Henriques 3, Ana Francisca Rozin Kleiner 4, Anderson Belgamo 5, André Santos Cabral 6, Anselmo Athayde Costa e Silva 7, Bianca Callegari 7,8, Givago Silva Souza 1,2,*
Editor: Manabu Sakakibara9
PMCID: PMC8049300  PMID: 33857169

Abstract

We investigated the impact of visual impairment on balance control. We measured the center of pressure (COP) between the two feet and plantar surface pressures on each foot in 18 normal-sighted participants and compared their data with measures from 18 legally blind participants, either acquired or congenital. Pressures were measured in open- and closed-eye conditions using a baropodometric resistive plate. In the eyes-open condition, there were no differences between the sighted and legally blind groups in COP displacement. However, participants with visual loss had significantly increased pressures in two metatarsal regions (M1 and M2 zones) of the plantar surface in both viewing conditions (p < 0.05). The differences in pressure measures between the normally sighted and legally blind groups could be attributed mainly to the subgroup of subjects with acquired impairment. Our findings suggest that subjects with visual impairment present increased metatarsal pressures (i.e. forefoot), not yet associated to anterior displacement of COP or impaired balance control.

Introduction

Dynamic maintenance of balance while standing in humans relies on information from visual, vestibular, and proprioceptive inputs required by the brain to appropriately generate the complex array of motor commands needed to achieve equilibrium in a standing position [1–4]. Sensory impairment can impede adaptive postural control mechanisms and lead to equilibrium loss (i.e., visual [5–7]; vestibular [8, 9]; proprioceptive [10, 11]; vestibular and proprioceptive [12]).

The contribution of the visual inputs to the balance control is a hot topic and have been previously investigated. Maintenance of balance control in conditions of visual loss is aided by vestibular and proprioceptive inputs and is manifested via compensatory adjustments of postural weighting [13, 14]. Since postural changes in standing position reflect modifications in our body weight load on the plantar surface, measurement of plantar pressure can be used to quantify the influence of visual input on posture control [15]. A variety of tools have been employed to quantify balance control, such as stabilometry, dynamometry, video system analysis, electromyography during the execution of quiet stance, tandem Romberg test, one leg stance, and reaction-time tasks [13, 14, 16–23].

Measuring postural control in subjects with sensory impairment can quantify the effects of the impairment on balance control mechanisms [6–12, 16, 23]. There are mixed findings regarding the impact of visual loss on balance control and equilibrium [6–12, 24–26]. Some research finds that people with visual deficits have impaired balance control [16, 17], while other research finds minor or no differences in static and dynamic postural control between sighted and visually impaired subjects [13, 18, 19, 27]. Subjects with altered binocular vision have been found to have significantly altered measures of foot plantar pressures, and blind subjects can have prolonged foot-to-ground contact during gait [15, 24].

One variable that could affect balance control is whether the visual function loss is congenital or acquired. Previous studies investigated balance control in subjects with congenitally and acquired blindness [28, 29] and reported no differences between control and congenitally blind individuals, but participants with acquired blindness were less stable than controls. Some studies suggest that individuals with congenital visual impairment develop effective somatosensory and vestibular mechanisms to compensate for a lack of visual information since the birth [13, 14].

In the present study we aimed to measure balance control by direct and indirect (plantar surface pressure distribution) measures of COP from congenitally and acquired blind subjects and compare these data with data from sighted subjects.

Based on prior data, we hypothesized that subjects with acquired visual impairment would be more susceptible to disturbances in balance control, and hence maintenance of normal COP, and that associated deficits would be found in the load of pressures on the plantar surface of the foot. However, it is not obvious which specific regions of an individual foot would manifest changes in balance control.

Methods

Ethical consideration

All procedures were approved by the Ethical Committee for Research in Humans of the Science Health Institute of the Federal University of Pará (report #3.040.281/2018) and followed the STROBE statement. Written informed consent was obtained from all the participants before the procedures start. The visually impaired subjects read a Braille version of the instructions document or were verbally instructed before giving consent. Data were acquired between December 2017 to September 2019.

Subjects

Our sample consisted of 36 subjects between 18 and 50 years-old (18 sighted participants, 18 visually impaired participants). The sample of legally blind subjects was recruited from the José Alvares de Azevedo school for the blind and visually impaired. Participants were not compensated financially. Inclusion criteria were impairment of the visual perception and no motor function disturbances to keep an erect posture. Exclusion criteria for both groups were somesthetic, orthopedic, or vestibular, and neurological pathologies, motor disturbances or attention and/or memory deficits.

An ophthalmologist evaluated all blind participants. We used an ETDRS chart (Xenonio, Brazil) to estimate the visual acuity. All sighted participants had normal or best-corrected visual acuity at 20/20. The visual acuity was recorded in Snellen fraction, and in the cases of very low vision (worse than 20/200), the visual acuity was classified using a semi-quantitative scale: counting fingers (CF), hand motion (HM), light perception (LP), and no light perception (NLP). After the ophthalmological examination and the history of the present illness we divided the sample into acquired and congenital blind participants. All blind subjects that participated in the present study were legally blind (i.e., visual acuity was equal to or worse than 20/200) (Table 1). The definition of blindness is based on foveal vision (central vision), and most of the blind participants had some luminance perception, indicating some peripheral visual function. It is unclear the role of central or peripheral vision in balance control, if both have equal importance, or if both have complementary functionality [30–34].

Table 1. Description of the visual deficits of the visually impaired participants.

Patient Diagnosis Blindness Visual acuity
P1 Glaucoma Congenital LP/LP
P2 Optic nerve atrophy Acquired (10 years ago) LP/LP
P3 Glaucoma Congenital HM 1.7’/CF 1.7’
P4 Pituitary adenoma Acquired (17 years ago) NLP/NLP
P5 Cataract Acquired (5 years ago) LP/LP
P6 ND Congenital NLP/NLP
P7 ON atrophy Acquired (13 years ago) LP/LP
P8 Uveitis Congenital NLP/NLP
P9 Cataract Congenital LP/LP
P10 Cataract Acquired (2 years ago) LP/LP
P11 Cataract Congenital LP/LP
P12 Chorioretinitis Acquired (30 years ago) 20/200/CF 3.5’
P13 ND Congenital LP/LP
P14 Retinitis pigmentosa Congenital LP/LP
P15 Glaucoma Congenital LP/LP
P16 Glaucoma Acquired (8 years ago) NLP/NLP
P17 Cataract Congenital LP/LP
P18 Glaucoma Acquired (3 years ago) LP/LP
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ND: not diagnosed; ON: Optic neuritis; LP: Light perception; NLP: No light perception; CF: Counting fingers; HM: Hand motion. The visual acuity descriptions for counting fingers or hand motion are expressed as the maximum distance, in feet, from which detection was successful.

Ten out of 18 visually impaired participants had congenital visual impairment, while 8 participants had acquired visual impairment. Four of the 18 blind participants had no light perception, while the others had visual acuities ranging from light perception to 20/200 visual acuity (Table 1).

Physical examination

Age, height, and weight information from all participants were collected. Table 2 describes the physical characteristics of the participants from both groups. All participants carried out a physical evaluation comprising a manual muscle testing on a five-point scale (0 –no muscle strength, 5 –maintain the position when a maximum resistance is applied), assessment for muscle tone, evaluation of superficial and deep reflexes, tactile sensitivity using a brush of the reflex hammer, vibration sense testing with a 128-Hz tuning fork, motor coordination evaluation using finger-to-nose test and motion of the heel over the shin test. For the physical examination test, all the participants had normal results.

Table 2. Physical characteristics of the groups.

Variable CG VIG p-value
Age (years) 31.8 ± 8.3 31.5 ± 9.4 0.90
BMI (kg/cm2) 25.4 ± 4.4 24.8 ± 5.1 0.73
Male/Female 12 M/ 6 F 13 M/ 5 F 0.99
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Values are present as means and standard deviations for age and BMI.

CG: control group; VIG: visually impaired group; BMI: body mass index.

Table 1 describes the physical features of the participants. Both groups were age-, body mass index- (BMI), and male/female proportion matched. The sample was homogeneous to age, BMI, and male/female proportion.

Apparatus and experimental procedures

All participants stood in normal quiet stance on a baropodometric resistive plate (EPS R-1 model, Loran Engineering, Italy) with 2224 sensors distributed over 48 cm2, with a pressure-range capacity of 50–350 kilo-Pascals (kPa), and a data-acquisition rate of 50 Hz. The individuals were barefoot, with feet held apart at a distance between the shoulders and arms lying along the lateral torso. Sighted participants were asked to direct their gaze to a circular target on the wall a 1 m distance. Visually impaired participants were requested to direct their gaze forward while standing 1 m away from the wall. Conversation was not allowed during the recording sessions, except for the orientations of the participants by the examiners. Simultaneous data acquisition of the center of pressure (COP) displacements and barefoot plantar pressures were performed using Biomech Studio software (Loran Engineering, Italy). Measurements were carried out in open and closed eye conditions, during three trials of 60 seconds in each condition, with 60 seconds of rest between open- and closed-eye conditions. COP displacements along the anteroposterior and mediolateral directions were exported and were used to quantify the postural stability using the parameters of total displacement (COPdistance) and the area of displacement ellipse (COParea) enclosed by the statokinesiogram [35].

Pressure (in kPa) measures from 10 zones of the plantar surface delimited by the Biomech Studio software (forefoot: T1 –zone of the first toe, hallux, T2-5 –zone between the second and fifth toes, M1, M2, M3, M4, and M5 zones–zone of the first, second, third, fourth, and fifth metatarsal heads, respectively; midfoot: MF zones; hindfoot: LH–lateral heel zone and MH–medial heel zone) were quantified as mean (Pmean), and maximum (Pmax) pressures obtained from three-time series [36]. A schematic representation for analyzing the indirect measure of the postural control based on plantar pressures is shown in Fig 1.

Fig 1. Representation of the zones of the foot where plantar pressures were quantified.

Fig 1

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Forefoot is represented by the T1 (first toe), T2-5 (2nd-5th toes), M1 (1st metacarpal), M2 (2nd metacarpal), M3 (3rd metacarpal), M4 (4th metacarpal), M5 (5th metacarpal) zones; Midfoot is represented by the MF zone; Hindfoot is represented by the medial (MH) and lateral zones (LH).

Data analysis

GraphPad Prism 8 (GraphPad software, Inc., CA, USA) was used to the data analysis. Normality of data was tested using the Shapiro-Wilk test. Non-normal distribution data from control and visually impaired groups were compared using the non-parametric Mann-Whitney U test. We also divided the legally blind group into congenital and acquired subgroups and compared their data to the control using the Kruskal-Wallis test followed by the Dunn post hoc test. We calculated the adjusted p-values for multiplicity using the Bonferroni correction. A Chi-square with Yates’ correction was used to compare the proportions of male and female participants of each group, and Student’s t-test was used to compare age, height, weight, and body mass index between groups. A significance level of 0.05 was considered for all the statistical procedures.

Results

Balance control comparisons

Typical statokinesiograms were found for all participants, in which anteriorposterior displacements are larger than the laterolateral displacements during the test duration. Fig 2 shows representative statokinesiograms obtained from one representative participant in each group, and no systematic or qualitative differences between the groups could be observed between the statokinesiograms of these participants. Table 3 presents the descriptive statistics for stabilometric variables in the different test conditions for control and visually impaired groups. Both groups’ balance control was similar as no significant difference was found between the sighted and the visually impaired groups for COPdistance and COParea in either open- and closed-eye conditions. Similarly, no significant difference for stabilometric parameters was found when comparing control, congenital, and acquired visually impaired subjects (Table 4).

Fig 2. Statokinesiogram of one representative participant from the sighted group and one representative participant from the blind group.

Fig 2

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Recordings from the sighted participant in the open-eye (A) and closed-eye condition (B), and from a visually impaired (blind) participant in the open-eye (C) and closed-eye (D) conditions.

Table 3. Comparison of stabilometric data obtained from control and visually impaired groups.

Variable CG LBG P
Open eye condition
COPdistance 327.46 (93) 311.23 (89.2) 0.99
COParea 87.69 (72.6) 68.33 (61.9) 0.86
Closed eye condition
COPdistance 351.3 (48.3) 319.75 (101.9) 0.42
COParea 110.64 (109.1) 73.66 (58.8) 0.5
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CG: control group; LBG: legally blind group.

Table 4. Comparison of the stabilometric parameters between control group and visually impaired group according to etiology of the impairment.

Legally blind group
Variable Control group Congenital Acquired p-value
Open eye condition
COPdistance 327.5 (103.8) 345.8 (140.1) 309.3 (75.2) 0.93
COPárea 87.7 (82.1) 69.03 (63.5) 66.82 (112.4) 0.84
Closed eye condition
COPdistance 351.3 (57) 336.6 (165.1) 317.7 (50.3) 0.53
COParea 110.6 (118.6) 66.59 (102.91) 92.04 (120.1) 0.43
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Plantar pressures comparisons

Fig 3 shows an example of a heatmap of the Pmean of the feet from the same representative participants shown in Fig 2. In the control participant (Fig 2A), we observed the distribution of pressures occurring mainly on the hallux and mid-to-lateral metatarsus and heel regions. In contrast, in the visually impaired participant, the pressures were mainly localized on between the hallux, metatarsal (M1-M5) region of the left foot, and the heel.

Fig 3. Heatmap of the plantar pressure measurements obtained from the participants whose balance control data are shown in Fig 2.

Fig 3

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(A) Sighted participant. The pressures are distributed from the hallux to mid-lateral foot and in the heel. (B) Visually impaired participant. The pressure distribution occurs mainly in the hallux, all the metatarsal region of the left foot and in the heel.

Table 5 compares the plantar pressures between sighted and visually impaired subjects for open- and closed-eye conditions. Blind participants had significantly higher Pmean and Pmax in the M1 and M2 zones (p<0.05), respectively. No significant differences were found among the plantar pressures recorded from sighted, congenital, and acquired visually impaired participants in open-eye conditions. However, in the closed-eye condition, we found that acquired visually impaired participants had significantly higher Pmean and Pmax plantar pressures than the controls in M1 and M2 zones, respectively (Table 6). No significant difference was found between controls and congenital visually impaired participants or between the two visual impairment groups.

Table 5. Comparison of Pmean and Pmax measured in the different foot regions of control and visually impaired participants.

Pmean
Open eye condition Closed eye condition
Region CG LBG p-value CG LBG p-value
T1 6.83 (13.2) 10.92 (13.8) 0.27 8.83 (14.4) 14.33 (13.5) 0.67
T2-5 3.17 (4.9) 5.16 (4.5) 0.12 3.75 (6.3) 5.58 (6.1) 0.32
M1 18.25 (9.2) 25.75 (16.8) 0.01 18.08 (6) 23.5 (14.4) 0.005
M2 27.08 (21.5) 33.75 (21.3) 0.12 27.33 (20.3) 34.25 (21.7) 0.06
M3 40.75 (21.7) 43.25 (19.6) 0.41 35.92 (19.9) 45.75 (24.9) 0.15
M4 43.92 (26.8) 48 (19.6) 0.44 39.5 (28) 46.5 (20.4) 0.87
M5 24 (24.7) 29.42 (13.6) 0.99 26.17 (22.5) 26.25 (13.8) 0.56
MF 11.58 (11) 13.83 (9.1) 0.12 12.33 (11.6) 14.83 (8.3) 0.3
MH 63.92 (18) 59.17 (18) 0.5 60.92 (22) 60.67 (22.2) 0.8
LH 63.17 (10.1) 57.83 (13.3) 0.36 59.42 (15.8) 56.17 (19.7) 0.83
Pmax
Open eye condition Closed eye condition
Region CG LBG p-value CG LBG p-value
T1 16.5 (43.8) 30 (44.4) 0.19 22.08 (51.8) 44.5 (41.1) 0.63
T2-5 6.5 (14.2) 10.92 (17.3) 0.2 7.67 (17.5) 14.25 (20.6) 0.3
M1 49.17 (29.8) 60.83 (41.3) 0.06 43.5 (19.7) 64 (44.8) 0.02
M2 62.25 (38.6) 81.33 (40.5) 0.03 58.83 (35.5) 82.17 (37) 0.02
M3 85.75 (46.7) 89.25 (38.1) 0.56 73.33 (40.4) 90.17 (42.8) 0.37
M4 87 (58.2) 90.92 (41.6) 0.94 79.08 (52.1) 86.83 (44.6) 0.97
M5 69.75 (67.9) 82 (37) 0.94 74.92 (62.8) 72.42 (38.9) 0.75
MF 36.17 (36.2) 39.25 (12.5) 0.59 41.92 (42.1) 38.5 (18.3) 0.63
MH 153.3 (38.8) 145.3 (36.5) 0.37 148.4 (39.2) 153.8 (55.6) 0.97
LH 149 (33.5) 141.9 (30.5) 0.41 140.8 (40.9) 146.9 (53.1) 0.96
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CG: Control group; LBG: Legally blind group. Comparisons in bold represent significant differences using a Mann-Whitney test.

Table 6. Comparison of the plantar pressures among controls, congenital and acquired visually impaired participants during eye aperture conditions.

Pmean
OPEN-EYE CONDITION CLOSED-EYE CONDITION
Legally blind group Legally blind group
Region Control group Congenital Acquired Control group Congenital Acquired
T1 6.83 (13.2) 9.25 (13.9) 13.5 (10.6) 8.83 (14.4) 8.58 (15) 15.67 (9.8)
T2-5 3.17 (4.9) 4.25 (3) 7.08 (8) 3.75 (6.33) 4.33 (7.2) 7.08 (4.7)
M1 18.25 (9.2) 25.75 (16) 25.08 (20.2) 18.08 (6) 23.08 (12.2) 24.17 (15.8)*
M2 27.08 (21.5) 33.67 (18.2) 34.83 (25.3) 27.33 (20.3) 34.25 (18) 36.92 (23.1)
M3 40.75 (21.7) 43.25 (23.9) 42 (23.7) 35.92 (19.9) 40.67 (25.08) 49.08 (29.6)
M4 43.92 (26.8) 46.83 (25.5) 47.67 (24.6) 39.5 (28) 42.42 (25) 48.67 (21.8)
M5 24 (24.7) 30.17 (10.9) 27.25 (18) 26.17 (22.5) 26.42 (19.5) 25.58 (11.8)
MF 11.58 (11) 13.5 (9.9) 14.33 (10.3) 12.3 (11.5) 12.3 (18.4) 16.42 (4.9)
MH 63.92 (18) 59.42 (19.4) 57.83 (18.8) 60.92 (21.7) 61.17 (24.8) 58.67 (19.2)
LH 60.75 (11.7) 57.83 (14.6) 57.83 (20.5) 59.42 (15.8) 57.67 (26.1) 53.92 (16.3)
Pmax
OPEN-EYE CONDITION CLOSED-EYE CONDITION
Legally blind group Legally blind group
Region Control group Congenital Acquired Control group Congenital Acquired
T1 17.58 (57.5) 23.83 (44.7) 43 (35.2) 22.08 (51.8) 25.42 (48.3) 48.92 (27.5)
T2-5 6.5 (14.2) 8.83 (9.4) 18.75 (32.8) 7.67 (17.5) 8.58 (19) 20.67 (19.8)
M1 49.17 (29.8) 63.92 (44.4) 65.83 (58.3) 43.5 (19.7) 59.25 (29.6) 70.33 (52.5)
M2 62.25 (38.7) 81.42 (36.3) 78.83 (43.7) 58.83 (35.5) 75.25 (35.3) 96.58 (52.5)**
M3 85.75 (46.7) 90.42 (44.6) 85.25 (46.7) 73.33 (40.4) 79.42 (45) 96.58 (52.5)
M4 87 (58.2) 87.67 (47.4) 96 (49.6) 79.08 (52.1) 82.5 (47) 94.25 (57.2)
M5 69.75 (67.9) 82 (37.7) 78.58 (49.7) 74.92 (62.7) 71.67 (46.5) 74.67 (34.8)
MF 36.17 (36.2) 41.25 (24) 46.75 (25.8) 41.92 (42.1) 36.33 (47.9) 43.17 (17.2)
MH 153.3 (38.8) 155.7 (33.8) 134.3 (52.9) 148.4 (39.2) 158.4 (58.1) 139.8 (45.8)
LH 149 (33.5) 150.5 (31.7) 135.9 (50.5) 140.8 (40.9) 150.3 (52.3) 135.2 (45.2)
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Comparisons in bold represent significant differences using Kruskal-Wallis test followed by Dunn’s post hoc test.

*Higher than the control group (Dunn’s test, p = 0.02).

**Higher than the control group (Dunn’s test, p = 0.04).

Discussion

This study compared stabilometric and baropodometric measurements between sighted subjects and with subjects with acquired and congenital blindness. Similar to prior investigations, we observed no significant difference of the stabilometric variables (COPdistance, COParea) across the groups, indicating the action of compensatory mechanisms in the balance control of the participants with visual impairment [27, 37].

Additionally, we also observed that most of the foot zones of the legally blind participants had no significant pressure differences compared to controls, except for the higher maximum pressures in the first and second metatarsal heads (M1 and M2 zones) in patients in the closed-eye condition. These differences could be attributed to the contribution of the acquired blind participants’ data [15]. The small number of significant differences indicates that mild disturbances in the motor control of the balance are present and maybe can be ignored in conventional evaluation of the balance.

Because of the similarity in COP measures obtained from participants with congenital or acquired blindness, a working hypothesis could be that the mean duration of acquired impairment (11 ± 9.2 years) was adequate for the development and consolidation of compensatory balance-control mechanisms.

However, against such a hypothesis, the presence of significant differences in metatarsal head pressures argues for an incomplete establishment of these mechanisms in the participants with acquired blindness. Congenitally blind subjects would have an opportunity to develop compensatory mechanisms during their development in early childhood, while the ability to develop compensatory mechanisms in acquired visual loss would depend on many factors, including age of onset relative to any possible critical periods, and duration of the visual impairment. Moreover, it is possible that qualitatively different compensatory mechanisms for balance control might be utilized in acquired vs congenital visual impairment.

Because we found that differences between the acquired and congenital blind groups in plantar pressures occurred mainly in the closed-eye condition, residual light perception (present in most of the acquired blind group) is a likely an important factor that assists in performance during the balance control task.

In addition, the visual system has more than one pathway to the brain; and conscious visual perception is generated in only one of these pathways (from retina to primary visual cortex, V1). However, other visual pathways could be contributing to the balance control even in visually impaired or blind subjects (for example from retina to superior colliculus or pulvinar nucleus), as has been observed in cases of so-called “blindsight” demonstrating residual vision in several visual diseases [38–40].

We found that subjects in the acquired blind group exhibited an anterior displacement of pressures in the metatarsal zones of the forefoot in order to maintain equilibrium. Such anterior pressure displacements can lead to reflex activation of the plantar flexors and evertors of the ankle [41] and an increase of vestibular and proprioceptive inputs to partially compensate for the lack of visual information [21, 28, 42]. However, proprioceptive compensatory mechanisms alone do not appear to be adequate. Ozdemir et al. [42] observed that visually impaired subjects with high proprioceptive acuity had worse postural control performance than sighted people. The increase of the plantar pressures in M1 and M2 zones when the visually impaired participants had their eyes closed could be interpreted as a compensatory response that would to augment proprioceptive input to avoid loss of balance control. The plantar pressures’ change seems to be an anticipatory adjustment before the changes in balance control.

Finally, the role of hapic cues in the foot must be considered in our subjects, since it was previously demonstrated less frequent head displacements in sighted subjects than in visually impaired subjects, in experiments using haptic cues derived from a cane’s contact [21].

The present study has limitations that must be considered. The sample of participants with acquired blindness is heterogeneous in terms of duration of visual loss, for example. We would hypothesize that a longer period of visual loss could increase the chances of developing compensatory mechanisms for vision loss. A comparison of the balance control in subjects with short- and long-term acquired visual loss could help clarify the role that duration of acquired visual loss might have in the development of compensatory mechanisms in the nervous system.

We concluded that acquired blindness alters the balance control mechanisms more the congenital blindness, as evidenced by the anterior displacement of the foot pressures observed in the acquired blind subjects. Development of more complete compensatory mechanisms in congenital impairment (vs acquired) are suggested as a possible explanation to the observed difference. Our findings suggest that acquired blind people need more attention concerning the risk of fall.

Supporting information

S1 Database

(XLSX)

Click here for additional data file. (25.7KB, xlsx)

Acknowledgments

This research received funding from the Amazon Paraense Foundation of Studies (FAPESPA, No. 2019/589349) and the Research Funding and the National Council of Research Development (CNPq/Brazil, No. 431748/2016-0). GS was CNPq Productivity Fellow (No. 310845/2018-1).

Data Availability

All relevant data are within the manuscript and its Supporting Information files.

Funding Statement

This study was supported by: APESPA, 2019/589349, Mr Anselmo Athayde Costa e Silva Conselho Nacional de Desenvolvimento Científico e Tecnológico (BR), 431748/2016-0, Mr Givago Silva Souza Conselho Nacional de Desenvolvimento Científico e Tecnológico, 310845/2018-1, Mr Givago Silva Souza. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Decision Letter 0

Manabu Sakakibara

11 Dec 2020

PONE-D-20-33643

CHANGES IN PLANTAR LOAD DISTRIBUTION IN VISUALLY-IMPAIRED SUBJECTS

PLOS ONE

Dear Dr. Souza,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Two experts in the field have carefully evaluated the manuscript entitled, "CHANGES IN PLANTAR LOAD DISTRIBUTION IN VISUALLY-IMPAIRED SUBJECTS". Their comments are appended below.

The first reviewer gave rather favorable comments but not satisfactory. The second referee pointed out the drawbacks need to be revised from all the aspect of the manuscript.

This Academic Editor advise the authors to be consulted with a professional English Editing service before submission.

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We look forward to receiving your revised manuscript.

Kind regards,

Manabu Sakakibara, Ph.D.

Academic Editor

PLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

Reviewer #2: Partly

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: No

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: No

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Thank you for the opportunity to review the manuscript titled "CHANGES IN PLANTAR LOAD DISTRIBUTION IN VISUALLY-IMPAIRED SUBJECTS" (PONE-D-20-33643). This is an interesting descriptive study on the consequences of visual deprivation on balance and plantar pressures.

The authors provide a brief but interesting introduction, but do not include all the current scientific evidence on the subject.

Below, I suggest a series of changes to improve the quality of the manuscript, which I beg you to take as constructive criticism:

1. It is easier to make changes and indicate specific errors if the text has numbered lines. It is a suggestion for future submits.

2. In the abstract, it is no longer clear from the beginning whether we are talking about "visually impairment subjects" or "blind people", since as the authors indicate at the end of the discussion, "blind subjects" is not equal to "visual impairment ". It is better to use the same word mark throughout the text.

3. There are recent studies on plantar pressure and balance in healthy subjects that may help to support certain results of this study. For example:

Sánchez-González, María Carmen et al. Visual Binocular Disorders and Their Relationship with Baropodometric Parameters: A Cross-Association Study. BioMed Research International Volume 2020, Article ID 6834591, 9 pages. DOI: 10.1155 / 2020/6834591. It would be nice to include recent articles like this to improve the introduction and discussion.

4. In the methodology, the selection criteria of the sample have not been described and the characteristics of the sample are not exactly detailed until Table 1 and 2. Where is the sample collected from? It is too striking that the sample is so homogeneous in relation to age and body mass index.

5. It talks about the two situations in which the "visually impairment" subjects are measured: with eyes open and closed, but, if they were blind, as you say later, why have these two situations been taken into account?

6. Improve the quality of Figure 1, it looks a little blurry. It would be interesting to explain what the different zones consist of in the same text and not in the figure legends.

7. It is also striking that the sample is divided almost in half into "acquired" and "congenital" visually impairment subjects. Was it done randomly or was it sampled of some kind to select them?

8. The ages at which vision was lost in the "acquired" group are very different (30 years vs 2 years), could this not affect the previous visual experience and therefore the results?

9. Figure 2, like Figure 1, should be explained in text to reduce the figure legend.

10. Could tables 6 and 7 be unified so that the results of P mean and P max can be equated?

11. The discussion must be improved, including references that can justify the results, as well as not generalizing the results (as in the first section) where it literally says "the visually impaired participants had higher pressure in the first and second metatarsals". This has not been the case in all cases, it would be necessary to specify and try to justify these findings. Be careful with generalizing as the sample is not too large.

12. Merge the references in the discussion.

13. The last paragraph that explains the blindness, should be explained much earlier in the text of the manuscript, including putting it in the sample and its selection.

Reviewer #2: In this study authors aimed to investigate the effects of visual impairment on postural stability, considering both the center of pressure outcomes and the plantar surface distribution. The paper is interesting but results have poor potential broader relevance, since most of them were not significant. Furthermore, there are several issues which will require your attention.

1. The English in the present manuscript is not of publication quality and requires an improvement. Please carefully proof-read spell check to eliminate grammatical errors. Some periods need also to be revised, like for example the following, in the “Abstract” section:

“We aimed to compare the center of pressure and pressure in the feet plantar surface measured by sighted and visually impaired subjects”

Or the following in the “Introduction” section:

“Visual, vestibular, and proprioceptive inputs inform those forces to the brain in order to reach the equilibrium status on a standing position”.

2. Most of the references used are older than five years. Authors should focus on recent papers, like the following ones:

“Caldani, S., Bucci, M. P., Tisné, M., Audo, I., Van Den Abbeele, T., & Wiener-Vacher, S. (2019). Postural instability in subjects with usher syndrome. Frontiers in Neurology, 10.”

“D'Antonio, E., Tieri, G., Patané, F., Morone, G., & Iosa, M. (2020). Stable or able? Effect of virtual reality stimulation on static balance of post-stroke patients and healthy subjects. Human movement science, 70, 102569.”

Alghadir, A. H., Alotaibi, A. Z., & Iqbal, Z. A. (2019). Postural stability in people with visual impairment. Brain and Behavior, 9(11), e01436.

3. The Introduction is not complete. It should establish the context of the research by summarizing current understanding and background information about the topic, stating the purpose of the work, briefly explaining the rationale and the methodological approach, and highlighting the potential outcomes your study can reveal. Authors should describe previous studies and report the main results obtained from them. On the basis of these they should formulate their hypotheses.

4. Methods: Authors should describe in details the inclusion/exclusion criteria considering also the motor impairments.

5. Methods: Authors wrote that the noise was avoided in the room during recordings. Please explain this point, adding details about the methodology applied in order to avoid noise.

6. Methods: How did the authors consider the differences between the kind of visual impairment?

7. Figure 1: The figure is not clear. Please add some details in order to clarify that the shape is depicting a foot. Authors should also add a legend of the different areas they are representing. The resolution of the figure should also be improved.

8. Figure 2: Authors should change the scale of the figure in order to clearly show the differences between the four cases represented. What do authors want to highlight with this figure? Please add some details in order to clarify this point.

9. Results: Authors should explain how they applied the reduction of the p-value in the post-hoc analysis in order to appropriately perform the statistical analysis.

10. Results: Most of the results are not significant. What does it mean?

11. The limitations of the study should be integrated in the paper.

12. The conclusion should be also integrated in the paper.

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

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Reviewer #1: No

Reviewer #2: Yes: Erika D'Antonio

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

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Attachment

Submitted filename: PONE.docx

Click here for additional data file. (14KB, docx)
PLoS One. 2021 Apr 15;16(4):e0249467. doi: 10.1371/journal.pone.0249467.r002

Author response to Decision Letter 0

3 Mar 2021

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

Reviewer #2: Partly

A. We have made substantial modifications in the manuscript addressing the reviewers’ suggestions. We hope that the new version can be clearer for the readers.

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: No

A. We added the suggestions for the statistics description.

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

A. Thanks.

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: No

A. A native English-speaker ed0ited the final version of the present manuscript.

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Thank you for the opportunity to review the manuscript titled "CHANGES IN PLANTAR LOAD DISTRIBUTION IN VISUALLY-IMPAIRED SUBJECTS" (PONE-D-20-33643). This is an interesting descriptive study on the consequences of visual deprivation on balance and plantar pressures.

The authors provide a brief but interesting introduction, but do not include all the current scientific evidence on the subject.

Below, I suggest a series of changes to improve the quality of the manuscript, which I beg you to take as constructive criticism:

1. It is easier to make changes and indicate specific errors if the text has numbered lines. It is a suggestion for future submits.

A. Thanks. We included the numbered lines in the new version.

2. In the abstract, it is no longer clear from the beginning whether we are talking about "visually impairment subjects" or "blind people", since as the authors indicate at the end of the discussion, "blind subjects" is not equal to "visual impairment ". It is better to use the same word mark throughout the text.

A. In the new version of the manuscript we referred to the participants of our study as legally blind subjects, while we used other qualification (such as visually impaired) when is referenced participants from other investigations as is described by them.

3. There are recent studies on plantar pressure and balance in healthy subjects that may help to support certain results of this study. For example:

Sánchez-González, María Carmen et al. Visual Binocular Disorders and Their Relationship with Baropodometric Parameters: A Cross-Association Study. BioMed Research International Volume 2020, Article ID 6834591, 9 pages. DOI: 10.1155 / 2020/6834591. It would be nice to include recent articles like this to improve the introduction and discussion.

A. Thanks for the indication. We added it to the manuscript as well as other recent articles.

4. In the methodology, the selection criteria of the sample have not been described and the characteristics of the sample are not exactly detailed until Table 1 and 2. Where is the sample collected from? It is too striking that the sample is so homogeneous in relation to age and body mass index.

A. We added more information about the sample in the Methods section as follows (Page 7, Line 136):

“Both groups were age-, body mass index- (BMI), and male/female proportion matched. The sample was homogeneous to age, BMI, and male/female proportion.”

5. It talks about the two situations in which the "visually impairment" subjects are measured: with eyes open and closed, but, if they were blind, as you say later, why have these two situations been taken into account?

A. We added sentences about it in the Methods and Discussion sections.

In Methods (Page 5, Line 110):

“All blind subjects that participated in the present study were legally blind (i.e., visual acuity was equal to or worse than 20/200) (Table 1). The definition of blindness is based on foveal vision (central vision), and most of the blind participants had some luminance perception, indicating some peripheral visual function. It is unclear the role of central or peripheral vision in balance control, if both have equal importance, or if both have complementary functionality [31-35].”

In Discussion section (Page 16, Line 269):

“Because we found that differences between the acquired and congenital blind groups in plantar pressures occurred mainly in the closed-eye condition, residual light perception (present in most of the acquired blind group) is a likely an important factor that assists in performance during the balance control task.

In addition, the visual system has more than one pathway to the brain; and conscious visual perception is generated in only one of these pathways (from retina to primary visual cortex, V1). However, other visual pathways could be contributing to the balance control even in visually impaired or blind subjects (for example from retina to superior colliculus or pulvinar nucleus), as has been observed in cases of so-called “blindsight” demonstrating residual vision in several visual diseases [39-41].”

6. Improve the quality of Figure 1, it looks a little blurry. It would be interesting to explain what the different zones consist of in the same text and not in the figure legends.

A. Done.

7. It is also striking that the sample is divided almost in half into "acquired" and "congenital" visually impairment subjects. Was it done randomly or was it sampled of some kind to select them?

A. The sample of legally blind subjects was recruited from the José Alvares de Azevedo school for the blind and visually impaired. Participants were not compensated financially. An ophthalmologist evaluated all blind participants and classified them as acquired or congenital blinds. We evaluated all the available students to include the large possible number of subjects in the sample. For luck, we had similar number of participants in both groups.

8. The ages at which vision was lost in the "acquired" group are very different (30 years vs 2 years), could this not affect the previous visual experience and therefore the results?

A. Thanks for the question. It is not possible to assert about it, but we consider that represents a limitation of the study. We added this observation in the Discussion section as follows (Page 15, Line 256).

“Because of the similarity in COP measures obtained from participants with congenital or acquired blindness, a working hypothesis could be that the mean duration of acquired impairment (11 ± 9.2 years) was adequate for the development and consolidation of compensatory balance-control mechanisms.

However, against such a hypothesis, the presence of significant differences in metatarsal head pressures argues for an incomplete establishment of these mechanisms in the participants with acquired blindness. Congenitally blind subjects would have an opportunity to develop compensatory mechanisms during their development in early childhood, while the ability to develop compensatory mechanisms in acquired visual loss would depend on many factors, including age of onset relative to any possible critical periods, and duration of the visual impairment. Moreover, it is possible that qualitatively different compensatory mechanisms for balance control might be utilized in acquired vs congenital visual impairment.”

9. Figure 2, like Figure 1, should be explained in text to reduce the figure legend.

A. Done (Page 9, Line 188):

“Typical statokinesiograms were found for all participants, in which anteriorposterior displacements are larger than the laterolateral displacements during the test duration. Figure 2 shows representative statokinesiograms obtained from one representative participant in each group, and no systematic or qualitative differences between the groups could be observed between the statokinesiograms of these participants.”

10. Could tables 6 and 7 be unified so that the results of P mean and P max can be equated?

A. Done.

11. The discussion must be improved, including references that can justify the results, as well as not generalizing the results (as in the first section) where it literally says "the visually impaired participants had higher pressure in the first and second metatarsals". This has not been the case in all cases, it would be necessary to specify and try to justify these findings. Be careful with generalizing as the sample is not too large.

A. Thanks for the suggestions. We rewrote the Discussion following the suggestion.

12. Merge the references in the discussion.

A. Done.

13. The last paragraph that explains the blindness, should be explained much earlier in the text of the manuscript, including putting it in the sample and its selection.

A. Thanks. We replaced to the Methods section (Page 5, Line 110).

Reviewer #2: In this study authors aimed to investigate the effects of visual impairment on postural stability, considering both the center of pressure outcomes and the plantar surface distribution. The paper is interesting but results have poor potential broader relevance, since most of them were not significant. Furthermore, there are several issues which will require your attention.

1. The English in the present manuscript is not of publication quality and requires an improvement. Please carefully proof-read spell check to eliminate grammatical errors. Some periods need also to be revised, like for example the following, in the “Abstract” section:

“We aimed to compare the center of pressure and pressure in the feet plantar surface measured by sighted and visually impaired subjects”

Or the following in the “Introduction” section:

“Visual, vestibular, and proprioceptive inputs inform those forces to the brain in order to reach the equilibrium status on a standing position”.

A. The new version of the manuscript was edited by an English native-speaker and we hope to be suitable for publication quality.

2. Most of the references used are older than five years. Authors should focus on recent papers, like the following ones:

“Caldani, S., Bucci, M. P., Tisné, M., Audo, I., Van Den Abbeele, T., & Wiener-Vacher, S. (2019). Postural instability in subjects with usher syndrome. Frontiers in Neurology, 10.”

“D'Antonio, E., Tieri, G., Patané, F., Morone, G., & Iosa, M. (2020). Stable or able? Effect of virtual reality stimulation on static balance of post-stroke patients and healthy subjects. Human movement science, 70, 102569.”

Alghadir, A. H., Alotaibi, A. Z., & Iqbal, Z. A. (2019). Postural stability in people with visual impairment. Brain and Behavior, 9(11), e01436.

A. Thanks for the indications. We added them to the manuscript.

3. The Introduction is not complete. It should establish the context of the research by summarizing current understanding and background information about the topic, stating the purpose of the work, briefly explaining the rationale and the methodological approach, and highlighting the potential outcomes your study can reveal. Authors should describe previous studies and report the main results obtained from them. On the basis of these they should formulate their hypotheses.

A. We rewrote the Introduction section following the suggestions.

4. Methods: Authors should describe in details the inclusion/exclusion criteria considering also the motor impairments.

A. We added more information about the inclusion/exclusion criteria in the Methods section (Page 5, Line 99).

5. Methods: Authors wrote that the noise was avoided in the room during recordings. Please explain this point, adding details about the methodology applied in order to avoid noise.

A. We changed the sentence. We wrote that no conversation was not allowed during the recording sessions in the Methods section (Page 8, Line 152) as follows:

“Conversation was not allowed during the recording sessions, except for the orientations of the participants by the examiners.”

6. Methods: How did the authors consider the differences between the kind of visual impairment?

A. We added a sentence about the differences between the kind of visual impairment in the Methods section as follows (Page 5, Line 108):

“After the ophthalmological examination and the history of the present illness we divided the sample into acquired and congenital blind participants.”

7. Figure 1: The figure is not clear. Please add some details in order to clarify that the shape is depicting a foot. Authors should also add a legend of the different areas they are representing. The resolution of the figure should also be improved.

A. We created a new Figure 1 following the suggestion.

8. Figure 2: Authors should change the scale of the figure in order to clearly show the differences between the four cases represented. What do authors want to highlight with this figure? Please add some details in order to clarify this point.

A. Done (Page 9, Line 188):

“Typical statokinesiograms were found for all participants, in which anteriorposterior displacements are larger than the laterolateral displacements during the test duration. Figure 2 shows representative statokinesiograms obtained from one representative participant in each group, and no systematic or qualitative differences between the groups could be observed between the statokinesiograms of these participants.”

Typical statikinesiograms were found for all participants, which anteriorposterior displacements are larger than the laterolateral displacements during the test duration. Figure 2 shows representative statokinesiograms obtained from one participant in each group, and no systematic or qualitative differences between the groups could be observed.

9. Results: Authors should explain how they applied the reduction of the p-value in the post-hoc analysis in order to appropriately perform the statistical analysis.

A. We added a sentence with explanation about the adjusted p-values as follows (Page 9, Line 180):

“We calculated the adjusted p-values for multiplicity using the Bonferroni correction.”

10. Results: Most of the results are not significant. What does it mean?

A. We included in the Discussion a sentence debating about the non-significant and significant results as follows (Page 15, Line 249):

“Additionally, we also observed that most of the foot zones of the legally blind participants had no significant pressure differences compared to controls, except for the higher maximum pressures in the first and second metatarsal heads (M1 and M2 zones) in patients in the closed-eye condition. These differences could be attributed to the contribution of the acquired blind participants' data [15]. The small number of significant differences indicates that mild disturbances in the motor control of the balance are present and maybe can be ignored in conventional evaluation of the balance.”

11. The limitations of the study should be integrated in the paper.

A. Done (Page 17, Line 296):

“The present study has limitations that must be considered. The sample of participants with acquired blindness is heterogeneous in terms of duration of visual loss, for example. We would hypothesize that a longer period of visual loss could increase the chances of developing compensatory mechanisms for vision loss. A comparison of the balance control in subjects with short- and long-term acquired visual loss could help clarify the role that duration of acquired visual loss might have in the development of compensatory mechanisms in the nervous system.”

12. The conclusion should be also integrated in the paper.

A. Done (Page 17, Line 303):

“We concluded that acquired blindness alters the balance control mechanisms more the congenital blindness, as evidenced by the anterior displacement of the foot pressures observed in the acquired blind subjects. Development of more complete compensatory mechanisms in congenital impairment (vs acquired) are suggested as a possible explanation to the observed difference. Our findings suggest that acquired blind people need more attention concerning the risk of fall.”

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If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: Yes: Erika D'Antonio

A. Thanks for both reviewers for the extensive evaluation. We hope that the new version has been improved for publication.

Attachment

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Decision Letter 1

Manabu Sakakibara

19 Mar 2021

CHANGES IN PLANTAR LOAD DISTRIBUTION IN LEGALLY BLIND SUBJECTS

PONE-D-20-33643R1

Dear Dr. Souza,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

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Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #2: Yes

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Reviewer #1: The authors have incorporated all the suggestions made, improving the content and the methodology. Now the manuscript is much more enriched and improved.

Reviewer #2: Authors have adequately addressed all the comments raised in a previous round of review and the manuscript is now acceptable for publication.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

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Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: Yes: Erika D'Antonio

Acceptance letter

Manabu Sakakibara

5 Apr 2021

PONE-D-20-33643R1

CHANGES IN PLANTAR LOAD DISTRIBUTION IN LEGALLY BLIND SUBJECTS

Dear Dr. Souza:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

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Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Manabu Sakakibara

Academic Editor

PLOS ONE

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