The effect of transcranial direct current stimulation on balance in healthy young and older adults: A systematic review of the literature

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The effect of transcranial direct current stimulation on balance in healthy young and older adults: A systematic review of the literature Hamzeh Baharlouei a, Maryam A. Saba a, Mohammad Jafar Shaterzadeh Yazdi a,∗, Shapour Jaberzadeh b a

Musculoskeletal Rehabilitation Research Center, Ahvaz Jundishapur University of Medical Sciences, Golestan Street, Ahvaz, Iran b Department of Physiotherapy, School of Primary and Allied Health Care, Faculty of Medicine, Nursing and Health Sciences, Monash University, Melbourne, Australia Received 10 November 2019; accepted 24 January 2020

KEYWORDS Balance; Older adults; Transcranial direct current stimulation; Young

∗

Summary Various studies have investigated the effect of noninvasive brain stimulation methods such as transcranial direct stimulation (tDCS) on postural control in healthy young and older adults. However, the use of different treatment protocols and outcome measures makes it difficult to interpret the research results. This systematic review provides a comprehensive overview of the current literature on the effect of tDCS on postural control. Nine databases were searched for papers assessing the effect of tDCS on postural control in young healthy and/or older adults. The data of included studies were extracted and methodological quality examined using PEDro. Sixteen studies met the inclusion criteria. The results showed that anodal tDCS (a-tDCS) of primary motor cortex may improve dynamic balance in young healthy individuals. In older adults, a-tDCS of dorsolateral prefrontal cortex and cerebellum showed a positive effect on dual task and dynamic balance, respectively. In conclusion, tDCS may improve both static and dynamic balance in younger and older adults. However, due to lack of consensus in the results, caution is required when drawing conclusions with regards to these findings. © 2020 Elsevier Masson SAS. All rights reserved.

Corresponding author. E-mail address: [email protected] (M.J. Shaterzadeh Yazdi).

https://doi.org/10.1016/j.neucli.2020.01.006 0987-7053/© 2020 Elsevier Masson SAS. All rights reserved.

Please cite this article in press as: Baharlouei H, et al. The effect of transcranial direct current stimulation on balance in healthy young and older adults: A systematic review of the literature. Neurophysiologie Clinique/Clinical Neurophysiology (2020), https://doi.org/10.1016/j.neucli.2020.01.006

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Introduction Postural control plays a major role in daily activities [1]. The maintenance of balance is controlled by the integration of sensory information [2] and complex interaction between musculoskeletal and neurological systems [3]. Falls are the leading cause of accidental injuries in older adults [4]. About one third of elderly subjects are prone to falls [5]. The association between impaired postural control and falling has been shown in some studies [1,6]. There are several noninvasive brain stimulation techniques, which are used as a therapy to improve postural control. Transcranial direct current stimulation (tDCS) is one such technique, which can be easily applied using a simple generator of the direct current [7,8]. According to ‘‘somatic doctrine’’, anodal tDCS (a-tDCS) induces inward current flow under the anode, leading to somatic depolarization and therefore enhances corticospinal excitability. On the other hand, cathodal tDCS (c-tDCS) induces an outward current leading to somatic hyperpolarization, which may lead to a decrease in corticospinal excitability. It should be noted that the effect of the tDCS montage depends on several factors including target area, spatial orientation of neurons with respect to stimulation and modifying factors such as different pathologies and drugs [9]. The effects of tDCS on the balance have been investigated among young healthy participants. These studies applied tDCS on several areas of brain including dorsolateral prefrontal cortex (DLPFC) [10], cerebellum [11,12], supplementary motor area (SMA) [13], primary motor cortex (M1) [11,14], vertex [15], primary sensory and motor cortex (PSMC) or posterior parietal cortex (PPC) [16]. Other studies have reported the effect of tDCS on DLPFC [17,18], M1 [11,19,20], or cerebellum [11,21] on balance in older adults. Recently, two systematic reviews addressed the effect of tDCS on balance control. Yadolahi et al. [22] synthesized studies that investigated this effect in populations of patients with neurological diseases, older adults and younger adults. However, the results were not segregated according to different methods used to measure postural control; e.g., static and dynamic balance and intervention protocols were not discussed in detail in this review. The study by de Moura et al. [23] dealt with the effect of tDCS on balance in healthy population without separately analyzing the results for static and dynamic balance. Despite the potential benefits of tDCS on balance, there are limited systematic reviews focused on this area of research. Moreover, there is heterogeneity in intervention protocols (e.g. cathodal vs anodal stimulation; area of brain stimulated) and outcome measures (static vs. dynamic balance) used to study the effect of tDCS balance. Considering the differences between static and dynamic balance [24], a systematic review is needed to highlight the most effective protocols based on different types of balance and the age of participants. The participants in these studies can be categorized into two age groups: older adults aged over 60 years and younger adults aged below 30 years. Therefore, the aim of this study was to systematically analyze studies that investigated the effects of tDCS on postural control in healthy young and older adults. The main questions in this review were as follows:

• Can tDCS improve static or dynamic balance in young people? • Can tDCS improve static or dynamic balance in older adults? • Which tDCS protocols have the greatest impact on postural control indices?

Methods Literature search Web of Science, Science Direct, PubMed, Scopus, Physiotherapy Evidence Database, Clinical Key, Cochrane Central Register of Controlled Trials, Ovid Medline and ProQuest were searched for relevant papers since inception until February 2018. The search was limited to papers published in English language using the following key terms: ‘‘postural control’’, ‘‘postural sway’’, ‘‘postural balance’’, ‘‘balance’’, ‘‘tDCS’’ and ‘‘transcranial Direct Current Stimulation’’. Reference lists of the included studies were also reviewed to capture additional eligible studies. Two reviewers (HB and MS) independently searched the databases to find the relevant studies.

Selection criteria Articles were included if they met the following criteria: • the population consisted of healthy people with the age of older participants being 60 years or older; • the intervention used in the study was tDCS; • the outcome measure of interest included any indices of balance and postural control. Articles were excluded if the language was non-English or the research involved individuals suffering from any systemic (e.g. diabetic mellitus) or neurologic disease (e.g., stroke, Parkinson’s). In addition, studies that applied tDCS with a combination of other techniques such as motor imagery were also excluded.

Data extraction The relevant data from the included studies were independently extracted by two authors (HB and MS). The extracted data captured methodological and technical considerations including trial design, number of participants, age, gender, experimental conditions, outcome measures and variables, results, drop out, number of tDCS sessions, duration (min/session) of applications, density of the applied current, stimulated area, the position, polarity and size of the electrodes, and tolerance/side/adverse effects of tDCS applications. Both authors agreed on the extracted data.

Quality assessment Both authors (HB, MS) independently assessed the methodological quality of selected studies using the Physiotherapy Evidence Database Scale (PEDro;

Please cite this article in press as: Baharlouei H, et al. The effect of transcranial direct current stimulation on balance in healthy young and older adults: A systematic review of the literature. Neurophysiologie Clinique/Clinical Neurophysiology (2020), https://doi.org/10.1016/j.neucli.2020.01.006

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tDCS effect on balance http://www.pedro.org.au/). The criteria of the PEDro scale are: • • • • • • • • •

• •

eligibility criteria specified; subjects randomly allocated to groups; allocation concealed; the groups being similar at baseline regarding the most important prognostic indicators; blinding of all subjects; blinding of all therapists who administered the therapy; blinding of all assessors who measured at least one key outcome; measures of at least one key outcome obtained from more than 85% of the subjects initially allocated to groups; all subjects for whom outcome measures were available received the treatment or control condition as allocated, or where this was not the case, data for at least one key outcome was analyzed by ‘‘intention to treat’’; results of between-group statistical comparisons reported for at least one key outcome; both point measures and measures of variability for at least one key outcome provided.

The first question is related to external validity and the subsequent criteria assess the internal validity. Therefore, the first item is not used to calculate the PEDro score [25,26]. The PEDro cut-points for determination of quality are 9—10 (excellent), 6—8 (good), 4—5 (fair) and below 4 (poor) [27].

Results Identification and selection of studies A total of 1582 articles was found in the initial search, including 383 duplicates. Screening the titles and abstracts excluded 1176 articles. Six articles were abstracts presented in scientific seminars; in one article tDCS was applied in combination with motor imagery [28], and in another one with balance training [29]. In the study by Poortvliet et al. [30], balance recovery was assessed following Achilles’ tendon vibration. Finally, 16 studies were selected for this study. They were published from 2014 to 2018 (Fig. 1).

Quality assessment The PEDro score of included studies was within the 5—9 range for all, indicating good quality (Table 1). In all studies except one [31], allocation was concealed [11—13,15,17,19,21,32,33] and seven studies were doubleblinded [10,11,16,18,20,21,31].

Participants in the included studies In total, 209 young and 168 older adults participated in the included studies with their age ranging within 20.81—26.4 years and 61—72.44 years respectively. In nine studies, the participants were young [10,12—16,31,32,34], in six studies, they were older adults [17—21,33], and in one study both young and older adults participated [11].

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Intervention In 12 studies [10,11,13—15,17—21,33,34] anodal and in 1 study [32] cathodal tDCS were used. The study by Inukai et al. [12] had two phases; in the first phase cathodal, anodal, and sham tDCS were applied in a random order, while in the second phase only cathodal tDCS was used. In two studies [16,31] anodal, cathodal, and sham tDCS were utilized. The study by Hupfeld et al. [13] was the only one without sham stimulation (Table 2). Some of the studies reported similar size of electrodes for both main and return electrodes [10,12—15,17,18,20,21,31,32], while in other studies the main electrode was smaller than the return electrode [11,14,16,19,33,34] (Table 2). The intensity of tDCS used in the included studies ranged from 0.5 to 2 mA, but in three studies comfortable sensation of the current by participants was used for adjustment of amplitude [10,17,18]. Although duration of tDCS application was 20 min in the majority of studies [10—12,14,15,18—21,32,35], a few studies used treatment times of 10 min [16], 15 min [33,34] and 85 min [13]. Foerster et al. [31] reported an application duration of 13 min for anodal and 9 min for cathodal stimulation (Table 2). The main electrode in the included studies was located over different sites as follows: cerebellum [11,12,16,21,31], M1 [11,14,19,20,34], DLPFC [10,17,18], vertex [15], SMA [13,33] and PSMC and PPC [32] (Table 2).

The effect of tDCS on balance The effect of tDCS on static balance in young people In 5 studies, the participants were younger adults and the outcome measure was based on static balance indices [10,12,15,31,32] (Table 3). Most of these studies reported results immediately after a-tDCS [10,12,31,32] while one study assessed the effect of tDCS during and 20 min after the intervention [15]. These studies reported that a-tDCS of cerebellum [12,31], M1 [15], DLPFC [10] or PSMC/PPC [32] could not improve static balance in young healthy people. However, lack of improvement was only demonstrated for single task condition with the CoP area and speed reduction in dual task condition following application of a-tDCS of DLPFC [10]. In a study by Foerster et al. [31], c-tDCS of cerebellum decreased static balance while in another study by Inukai et al. [12] this application had a positive effect on static balance. In general, these sparse pieces of evidence did not support the effect of tDCS on static balance in young healthy adults. The effect of tDCS on dynamic balance in young people Six studies reported the effect of tDCS on dynamic balance in healthy young adults (Table 4) [11,13,14,16,31,34]. Four studies measured balance during stimulation [11,13,14,16], with four studies reported the immediate effect of tDCS [11,13,31,34]. In one, post 30 [11] and in another one post 45 and post 60 [34] minutes were retesting times, and two studies assessed the retention effect one day after intervention [14,16].

Please cite this article in press as: Baharlouei H, et al. The effect of transcranial direct current stimulation on balance in healthy young and older adults: A systematic review of the literature. Neurophysiologie Clinique/Clinical Neurophysiology (2020), https://doi.org/10.1016/j.neucli.2020.01.006

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Figure 1

Flowchart of study selection stage.

Some studies showed that a-tDCS of M1 [11,14,34], SMA [13] or cerebellum [11] could improve dynamic balance in young people. However, the effect of cerebellar stimulation on dynamic balance was borderline [11]. Two studies reported that neither anodal nor cathodal stimulation of cerebellum had any effect on dynamic balance in younger adults [16,31]. In conclusion, current evidence suggests that a-tDCS of M1 for 20 min with a current density of 0.04 mA/cm2 improves dynamic balance in young healthy people. The effect of tDCS on static balance in older adults Only three studies assessed the effect of tDCS on static balance in older adults (Table 5) [17,18,21]. All three studies measured balance immediately after intervention

[17,18,21], while one study beside the immediate effect, reported the effect 48 hours later [21]. Ehsani et al. [21] showed that cerebellar a-tDCS improves anterioposterior and mediolateral stability along with Berg balance scale scores in older adults. Two other studies which assessed the effect of a-tDCS of DLPFC on static balance in older adults revealed that tDCS may improve the dual task balance but with no effect on static balance during the single task condition [17,18]. Since there are very few studies reporting the effect of tDCS on static balance in older adults, drawing a firm conclusion in this area is almost impossible. In general, 20 min of a-tDCS of DLPFC with 2 mA intensity has immediate effect on the balance scores in older adults during dual task conditions.

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Dutta 2014

Ehsani 2017

Foerster Hupfeld 2017 2016

Inukai 2016

Ishigaki 2016

Kaminski 2016

Kaminski 2017

Lee 2012

Manor 2016

Nomura 2018

Steiner Zhou 2016 2014

Zhou 2015

Zhou 2018

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Craig 2017

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Quality assessment of included studies.

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1 2 3 4 5 6 7 8 9 10 11 Total score

tDCS effect on balance

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Table 1

1 — Eligibility criteria were specified. 2 — Subjects were randomly allocated to groups. 3 — Allocation was concealed. 4 — The groups were similar at baseline regarding the most important prognostic indicators. 5 — There was blinding of all subjects. 6 — There was blinding of all therapists who administered the therapy. 7 — There was blinding of all assessors who measured at least one key outcome. 8 — Measures of at least one key outcome were obtained from more than 85% of the subjects initially allocated to groups. 9 — All subjects for whom outcome measures were available received the treatment or control condition as allocated or, where this was not the case, data for at least one key outcome was analyzed by ‘‘intention to treat’’. 10 — The results of between-group statistical comparisons are reported for at least one key outcome the results of between-group statistical comparisons are reported for at least one key outcome. 11 — The study provides both point measures and measures of variability for at least one key outcome.

5

Main electrode

Electrode size (cm2 )

Intensity (mA)

Current density (mA/cm2 )

Duration of application (min)

Site of stimulation

Craig 2017

Anode

2

0.04

20

Dutta 2014 Ehsani 2017 Foerster 2017

Anode Anode Anode, cathode

M = 50, R = 25 M = 9, R = 35 M = R = 25 M = R = 25

0.5 1.5 1

0.06 0.06 0.04

Hupfeld 2016

Anode

M = R = 25

Inukai 2016 Ishigaki 2016 Kaminski 2016 Kaminski 2017

Anode, cathode Cathode Anode Anode

Lee 2012 Manor 2016 Nomura 2018 Steiner 2016

Anode Anode Anode Anode, cathode

Zhou 2014 Zhou 2015 Zhou 2018

Anode Anode Anode

M = R = 35 M = R = 35 M = R = 25 M = 25, R = 50 M = R = 35 M = R = 35 M = 9, R = 35 M = 35, R = 25 M = R = 35 M = R = 35 M = R = 35

120 mA min (40 mA*3 days − 0.4 mA × ∼90 min) 2 0.06 1.5 0.04 1 0.04 0.04 1

15 20 Anodal: 13 min cathodal: 9 min Up to 85

Cerebellum, M1 M1 Cerebellum Cerebellum

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Study

SMA

20 20 20 20

Cerebellum PSMC, PPC M1 M1

2 2 2 2

0.06 0.06 0.22 0.06

20 20 15 10

M1 DLPFC SMA Cerebellum

1.5 2 2

0.04 0.06 0.06

20 20 20

DLPFC DLPFC M1

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Characteristics of tDCS.

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tDCS: transcranial direct stimulation; M: main electrode; R: reference electrode; PSMC: primary sensory motor cortex; PPC: posterior parietal cortex; DLPFC: dorsolateral prefrontal cortex; SMA: supplementary motor area.

H. Baharlouei et al.

Please cite this article in press as: Baharlouei H, et al. The effect of transcranial direct current stimulation on balance in healthy young and older adults: A systematic review of the literature. Neurophysiologie Clinique/Clinical Neurophysiology (2020), https://doi.org/10.1016/j.neucli.2020.01.006

Table 2

No. of participants

Age (years) Mean (SD)

Gender (male, female)

Measurement tool/outcome measure(s)

Measurement time

Results

Conclusion

Foerster 2017

Double-blinded cross over

15

21—24

0, 15

Overall stability index

Before, immediately after

Overall stability index: ↑ after c-tDCS and → after a-tDCS

Inukai 2016

Single-blinded Cross over

16

21 (2.9)

16, 0

Center of gravity sway

Before and after

Single group

Subgroup of 5

24.60 (2.61)

5, 0

Single-blinded Cross over design in two independent groups

Primary sensorimotor cortex (10)

24.2 (3.1)

5, 5

Stabilometer: postural sway

Before, after

Total locus length and Locus length per second: ↓ after c-tDCS and → after a-tDCS Total locus length and Locus length per second: ↓ Rectangular area and enveloped area: → Root mean square of ML and AL: →

C-tDCS: ↓ balance a-tDCS: → balance c-tDCS: ↑ balance a-tDCS: → balance ↑ balance

Posterior parietal cortex (10) a-tDCS, n = 15

23.4 (3.1)

6, 4

21.8 (1.3)

5, 10

Biodex Balance System SD: stability index in single leg stance position

Before, during, after 20 min walking on treadmill

Overall and AP stability indexes during stimulation and after 20 min treadmill walking: ↑ in both a-tDCS and sham groups ML stability index: ↑ in a-tDCS group, → in sham group

→ balance

21.4 (1.5)

4, 11

22 (2)

10, 10

Force plate: CoP speed and area Single and dual task conditions

Immediately before and after

Single task condition: → CoP speed and CoP area Dual task condition: ↓ CoP speed and CoP area

Single task condition: → balance Dual task condition: ↑ balance

Ishigaki 2016

Lee 2012

Zhou 2014

Single-blinded Randomized controlled trials

Double-blinded Cross over

Sham tDCS, n = 15 20

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Study design

→ balance

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a-tDCS: anodal transcranial direct current stimulation; c-tDCS: cathodal transcranial direct current stimulation; CoP: center of pressure; AP: anterioposterior; CoM: center of mass; ML: mediolateral; ↑: increase; ↓: decrease; →: no effect.

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Study

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Characteristics of included studies (younger adults, static balance).

tDCS effect on balance

Please cite this article in press as: Baharlouei H, et al. The effect of transcranial direct current stimulation on balance in healthy young and older adults: A systematic review of the literature. Neurophysiologie Clinique/Clinical Neurophysiology (2020), https://doi.org/10.1016/j.neucli.2020.01.006

Table 3

Study design

No. of participants

Age (years) Mean (SD)

Gender (male, female)

Measurement tool/outcome measure(s)

Measurement time

Results

Conclusion

Craig 2017

Doubleblinded Cross over

22

20.81 (2.07)

6, 10

Smart Balance Master (NeuroCom International): CoP trajectory over time in AP direction, AP path length, peak to peak away amplitude, mean power frequency of AP sway OE and CE conditions

Before, during, immediately after and 30 minutes after a-tDCS

↑ balance

Dutta 2014

Singleblinded Cross over

5

26.4 (5.3)

Wii Balance Board: CoM-CoP posturography, maximum excursions of CoP, reaction time during return to the center position

Before, immediately after, 45 min and 60 min after

Foerster 2017

Doubleblinded Cross over Singleblinded Cross over

15

21—24

0, 15

Biodex balance system Limits of stability

Before, immediately after

AP path length: → in CE and OE conditions and all four times of measurements Peak to peak sway amplitude: ↓ in CE condition from pre-test to post 0 and pre-test to post 30 Mean power frequency: ↑ in CE and OE conditions 30 min after cerebellar stimulation Maximum CoP excursion: ↓ Return reaction time: → Centroid of CoP: ↑ at 45 min and 60 min post tDCS Sway area: ↓ at 45 min and 60 min post tDCS CoP path length: ↓ at 60 min post tDCS Limit of stability: →

20

20—22

7, 13

Biodex balance system Limits of stability

Singleblinded Randomized, shamcontrolled Doubleblinded Randomized clinical trial

26

26.04 (3.14)

13, 13

Stability platform: time in balance, root mean square error

Before, during and after stimulation in three consecutive days During stimulation, one day after

30 10 participants in each group

23.7 (2.4)

15, 15

Lafayette Instrument 16030 stability platform: mean platform angle deviation and mean balance time

Hupfeld 2016

Kaminski 2016

Steiner 2016

↑ balance

→ balance

Balance time: ↑ Balance accuracy: →

↑ balance

Time in balance: ↑ during stimulation, → on day after Root mean square error: ↓ during stimulation, → one day after ↑ balance time and ↓ men platform angle in all three groups (anodal, cathodal and sham stimulation) in both day 1 and day 2

↑ balance

→ balance

a-tDCS: anodal transcranial direct current stimulation; c-tDCS: cathodal transcranial direct current stimulation; OE: opened eye; CE: closed eye; CoP: center of pressure; AP: anterioposterior; CoM: center of mass; ML: mediolateral; ↑: increase; ↓: decrease; →: no effect

H. Baharlouei et al.

During training on day 1 only Retention were tested on the next day

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Study

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Characteristics of included studies (younger adults, dynamic balance).

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Table 4

Study design

No. of participants

Age (years) Mean (SD)

Gender (male, female)

Measurement tool/outcome measure(s)

Measurement time

Results

Conclusion

Ehsani 2017

Double-blinded Randomized, shamcontrolled

29

65.79 (6.11)

13, 16

Biodex balance system: AP, ML and overall stability index, Berg balance scale

Before and immediately and 48 h after stimulation

↑ balance

Manor 2016

Single-blinded Cross over

37

61 (5)

12, 25

Force plate: average speed and area of postural sway Dual and single task

Before and after

Zhou 2015

Double-blinded Cross over

20

63 (3.6)

11, 9

Force plate: CoP complexity Single and dual task

Immediately before and after either real or sham tDCS

↑ AP and ML stability indexes, and berg balance scale → overall stability index Single task condition: → postural sway area and speed Dual task condition: ↓ postural sway area and speed Single task condition: → CoP complexity Dual task condition: ↓ CoP complexity

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Study

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Characteristics of included studies (older adults, static balance).

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tDCS effect on balance

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Table 5

Single task condition: → balance Dual task condition: ↑ balance

Single task condition: → balance Dual task condition: ↑ balance

a-tDCS: anodal transcranial direct current stimulation; c-tDCS: cathodal transcranial direct current stimulation; OE: opened eye; CE: closed eye; CoP: center of pressure; AP: anterioposterior; CoM: center of mass; ML: mediolateral; ↑: increase; ↓: decrease; →: no effect.

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10 The effect of tDCS on dynamic balance in older adults Dynamic balance in older adults was assessed in five studies (Table 6) [11,19—21,33]. Two studies reported the online effect of tDCS [11,19] and four studies measured balance immediately after the intervention [11,20,21,33]. In some studies, the balance was assessed 15 min [33], 30 min [11], 1 day [19], and 2 days [21] following tDCS. Some studies demonstrated that a-tDCS of cerebellum [11,21] or SMA [33] had a positive effect on dynamic balance in older adults. Regarding the effect of a-tDCS of M1 on dynamic balance in older adults, Craig and Doumas [11] reported modification in the measured indices. However, two other studies showed that anodal stimulation of M1 could not improve dynamic balance in older adults [19,20]. However there are limited evidences to support the positive effect of a-tDCS of cerebellum on dynamic balance in older adults. In general, there is lack of evidence to confirm beneficial effect of M1 a-tDCS on dynamic balance in older adults.

Side effects and attrition The side effects of tDCS were not reported in six studies [11,12,15,16,33,34]. The remaining studies showed that tDCS did not induce any side effects [10,13,14,17—21,31,32].

H. Baharlouei et al. balance measurement was not challenging enough to represent the difference between pre- and post-intervention (floor effect). Lee et al. [15] observed balance improvement in both intervention and control groups, while there was no difference between groups. In two other studies, the target areas were PSMC and PPC [32] and DLPFC [10], which may have no effect on postural control in healthy people. In general, it seems that there is a lack of evidence on the effect of tDCS on static balance in young people. Future research should focus on balance-specific brain regions and also use more sensitive outcome measures.

The effect of tDCS on dynamic balance in young people All three studies assessing the effect of a-tDCS of M1 on dynamic balance in younger adults reported positive findings [11,14,34]. M1 is part of the frontal cortico-basal ganglia network, which has a significant role in postural control [40]. Some studies demonstrated enhanced corticospinal [43,44] and spinal network [45] activity with a-tDCS over M1, which could impact balance-related reflexes [41]. Since postural sway is controlled by leg muscles [46], balance improvement could have been induced by the positive effect of a-tDCS on performance of the leg muscles [42]. Accordingly, it seems that facilitation of neurons in M1 by a-tDCS could be a useful technique for improving dynamic balance in young people.

Discussion The effect of tDCS on static balance in older adults Due to large heterogeneity in study designs, measurement tools and statistical models, meta-analysis was not possible in this review. However, a qualitative approach was used to classify the data and offer a number of clinical and experimental recommendations. Despite the diversity in target areas, most studies applied tDCS over cerebellum [11,12,16,21,31] or M1 [11,14,19,20,34]. The cerebellum integrates balance information [36,37], coordinates motor tasks [38] and controls postural stability [39]. Previous studies showed the role of M1 in the frontal cortico-basal ganglia network [40], balance-related reflexes [41] and performance of the leg muscles [42]. In most included studies, balance was assessed by laboratory tools. Since these tools are not available in physiotherapy clinics and might not provide an accurate picture of balance control at activity level, any generalization of findings to balance and falling in real life should be made with caution.

The effect of tDCS on static balance in young people Two studies on cerebellar and one study on M1 stimulation indicated that a-tDCS did not improve static balance in younger adults [12,15,31]. However, there were a number of methodological flaws in these studies. For instance, despite the importance of cerebellar vermis in standing postural balance, Foerster et al. [31] placed the anodal electrode on the right hemisphere rather than on the vermis. In a study by Inukai et al. [12], the selected task for

Two studies claimed that a-tDCS on DLPFC could improve dual task balance in older adults [17,18]. Performing multiple tasks simultaneously could enhance the activity of DLPFC [47], which plays an important role in the control of human posture during standing [48]. Based on the ‘‘bottleneck theory’’, dual task conditions are processed serially, in a way that during the processing of one task, the processing for the other task will be delayed [49]. The ‘‘capacity sharing theory’’, the other theory explaining the dual task activity, suggests that because of sharing cognitive resources, performance ability may decrease in at least one of the tasks [50]. Facilitation of DLPFC by a-tDCS may increase the speed of processing, thus improving postural control. As such, atDCS on DLPFC may optimize the availability and allocation of resources to the tasks [51]. In conclusion, while there is lack of evidence to support the effect of tDCS on static balance in older adults in single task conditions, it seems that a-tDCS of DLPFC could improve dual task static balance in older adults.

The effect of tDCS on dynamic balance in older adults Five studies were reviewed to answer whether tDCS could improve dynamic balance. It seems that a-tDCS of cerebellum could improve dynamic balance in older adults. The cerebellum has an important role in postural coordination since the sensorimotor information including proprioception, visual, and vestibular is integrated and re-weighted in this region [36,37]. In addition, functional connectivity

Please cite this article in press as: Baharlouei H, et al. The effect of transcranial direct current stimulation on balance in healthy young and older adults: A systematic review of the literature. Neurophysiologie Clinique/Clinical Neurophysiology (2020), https://doi.org/10.1016/j.neucli.2020.01.006

No. of participants

Age (years) Mean (SD)

Gender (male, female)

Measurement tool/outcome measure(s)

Measurement time

Results

Conclusion

Craig 2017

Double-blinded Cross over

20

72.44 (4.03)

4, 12

Smart Balance Master (NeuroCom International): CoP trajectory over time in AP direction, AP path length, peak to peak away amplitude, mean power frequency of AP sway OE and CE conditions

During, immediately after and 30 minutes after a-tDCS

↑ balance

Ehsani 2017

Double-blinded Randomized, shamcontrolled

29

65.79 (6.11)

13, 16

Biodex balance system: AP, ML and overall stability index, Berg balance scale

Before and immediately and 48 h after stimulation

Kaminski 2017

Single-blinded Randomized, controlled trials Cross over

30

13, 17

Stability platform: time in balance

During, one day after stimulation

12

72 (5.3)

4, 8

Dynamic balance Force plate: root mean square area, sway path length, ML and AP mean velocity

Before, immediately and 15 min after stimulation

Double-blinded Cross over

20

61 (4)

Not reported

Dynamic balance, Timed Up and Go

Immediately before and after either real or sham tDCS

AP path length: → in CE and OE conditions and all four times of measurements Peak to peak sway amplitude: ↓ in OE condition from pre-test to post0, → in CE condition Mean power frequency: ↓ from pre-stimulation to post 30 ↑ AP and ML stability indexes, and berg balance scale → overall stability index Time in balance: ↑ in both a-tDCS and sham groups during and one day after stimulation AP mean velocity: ↓ in immediately and 15 min after stimulation Sway path length: ↓ in immediately and 15 min after stimulation ML mean velocity and root mean square: → Timed Up and Go (s): →

Nomura 2018

Zhou 2018

67.7 (6)

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Study design

+Model

Study

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Characteristics of included studies (older adults, dynamic balance).

tDCS effect on balance

↑ balance

→ balance

↑ balance

→ balance

a-tDCS: anodal transcranial direct current stimulation; c-tDCS: cathodal transcranial direct current stimulation; OE: opened eye; CE: closed eye; CoP: center of pressure; AP: anterioposterior; CoM: center of mass; ML: mediolateral; ↑: increase; ↓: decrease; →: no effect.

11

Please cite this article in press as: Baharlouei H, et al. The effect of transcranial direct current stimulation on balance in healthy young and older adults: A systematic review of the literature. Neurophysiologie Clinique/Clinical Neurophysiology (2020), https://doi.org/10.1016/j.neucli.2020.01.006

Table 6

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12 between the cerebellum and motor cortex plays an important role in cognitive and motor tasks [38]. The vermis also contributes to control of postural stability by tuning the axial muscle activity [39]. It should be noted that the aging process changes the structure of the cerebellum, including reduction of white matter structural integrity and vermis volume, which may lead to balance and gait problems [52,53]. Anodal tDCS may facilitate the connectivity between the motor cortex and the cerebellum, which could lead to improved information processing and postural control [39]. Anodal tDCS of cerebellum could enhance the activity of Purkinje cells and facilitate the function of vermis and related white matter [54]. In addition, a-tDCS of cerebellum may affect cerebellar connection with the rest of the brain and improve vestibular and balance-related motor functions [55,56]. Therefore, cerebellar a-tDCS could be suggested for enhancing dynamic balance in older adults.

Conclusion Transcranial direct current stimulation is a safe method, which could improve postural control. In younger adults, a-tDCS of M1 could improve dynamic balance. Similarly, in older adults, a-tDCS of DLPFC and cerebellum have positive effects on postural control. Note that the positive findings on DLPFC were only reported in static dual task conditions and that cerebellar stimulation could improve only dynamic balance. However, published studies are limited and there are many controversies on the findings of studies. Therefore, caution should be employed when drawing any conclusion on the mentioned treatment protocols.

Limitations The conclusions in this study were mainly based on the studies written in English in peer-reviewed journals, while gray literature references such as theses and conference papers along with studies published in non-English languages were not included.

Disclosure of interest The authors declare that they have no competing interest.

Funding This work was supported by grants from the Musculoskeletal Rehabilitation Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran (grant number: PHT-9735).

Acknowledgments We thank Dr. Masood Mazaheri from the Centre of Precision Rehabilitation for Spinal Pain (CPR Spine), School of Sport, Exercise and Rehabilitation Sciences, College of Life and Environmental Sciences, University of Birmingham, for providing helpful comments on the manuscript.

H. Baharlouei et al.

References [1] Pollock AS, Durward BR, Rowe PJ, Paul JP. What is balance? Clin Rehabil 2000;14:402—6. [2] Peterka R. Sensorimotor integration in human postural control. J Neurophysiol 2002;88:1097—118. [3] da Silva FTG, Browne RAV, Pinto CB, Saleh Velez FG, do Egito EST, do Rêgo JTP, et al. Transcranial direct current stimulation in individuals with spinal cord injury: assessment of autonomic nervous system activity. Restor Neurol Neurosci 2017;35:159—69. [4] Noll DR. Management of falls and balance disorders in the elderly. J Am Osteopath Assoc 2013;113:17—22. [5] Gringauz I, Shemesh Y, Dagan A, Israelov I, Feldman D, PelzSinvani N, et al. Risk of falling among hospitalized patients with high modified Morse scores could be further Stratified. BMC Health Serv Res 2017;17:721. [6] Hubli M, Dietz V, Schrafl-Altermatt M, Bolliger M. Modulation of spinal neuronal excitability by spinal direct currents and locomotion after spinal cord injury. Clin Neurophysiol 2013;124:1187—95. [7] Bolognini N, Pascual-Leone A, Fregni F. Using non-invasive brain stimulation to augment motor training-induced plasticity. J Neuroeng Rehabil 2009;6:8. [8] Jeffery DT, Norton JA, Roy FD, Gorassini MA. Effects of transcranial direct current stimulation on the excitability of the leg motor cortex. Exp Brain Res 2007;182:281—7. [9] Lefaucheur J-P, Wendling F. Mechanisms of action of tDCS A brief and practical overview. Neurophysiol Clin 2019;49:269—75. [10] Zhou J, Hao Y, Wang Y, Jor’dan A, Pascual-Leone A, Zhang J, et al. Transcranial direct current stimulation reduces the cost of performing a cognitive task on gait and postural control. Eur J Neurosci 2014;39:1343—8. [11] Craig CE, Doumas M. Anodal transcranial direct current stimulation shows minimal, measure-specific effects on dynamic postural control in young and older adults: a double blind, sham-controlled study. PLoS One 2017;12:e0170331. [12] Inukai Y, Saito K, Sasaki R, Kotan S, Nakagawa M, Onishi H. Influence of transcranial direct current stimulation to the cerebellum on standing posture control. Front Hum Neurosci 2016;10:325. [13] Hupfeld KE, Ketcham CJ, Schneider HD. Transcranial direct current stimulation (tDCS) to the supplementary motor area (SMA) influences performance on motor tasks. Exp Brain Res 2016;235:851—9. [14] Kaminski E, Steele CJ, Hoff M, Gundlach C, Rjosk V, Sehm B, et al. Transcranial direct current stimulation (tDCS) over primary motor cortex leg area promotes dynamic balance task performance. Clin Neurophysiol 2016;127: 2455—62. [15] Lee YS, Yang HS, Jeong CJ, Yoo YD, Jeong SH, Jeon OK, et al. The effects of transcranial direct current stimulation on functional movement performance and balance of the lower extremities. J Phys Ther Sci 2012;24:1215—8. [16] Steiner KM, Enders A, Thier W, Batsikadze G, Ludolph N, Ilg W, et al. Cerebellar tDCS does not improve learning in a complex whole body dynamic balance task in young healthy subjects. PLoS One 2016;11:e0163598. [17] Manor B, Zhou J, Jor’Dan A, Zhang J, Fang J, Pascual-Leone A. Reduction of dual-task costs by noninvasive modulation of prefrontal activity in healthy elders. J Cogn Neurosci 2016;28:275—81. [18] Zhou D, Zhou J, Chen H, Manor B, Lin J, Zhang J. Effects of transcranial direct current stimulation (tDCS) on multiscale complexity of dual-task postural control in older adults. Exp Brain Res 2015;233:2401—9.

Please cite this article in press as: Baharlouei H, et al. The effect of transcranial direct current stimulation on balance in healthy young and older adults: A systematic review of the literature. Neurophysiologie Clinique/Clinical Neurophysiology (2020), https://doi.org/10.1016/j.neucli.2020.01.006

+Model NEUCLI-2691; No. of Pages 13

ARTICLE IN PRESS

tDCS effect on balance [19] Kaminski E, Hoff M, Rjosk V, Steele CJ, Gundlach C, Sehm B, et al. Anodal transcranial direct current stimulation does not facilitate dynamic balance task learning in healthy old adults. Front Hum Neurosci 2017;11:16. [20] Zhou J, Lo O-Y, Lipsitz LA, Zhang J, Fang J, Manor B. Transcranial direct current stimulation enhances foot sole somatosensation when standing in older adults. Exp Brain Res 2018;236:795—802. [21] Ehsani F, Samaei A, Zoghi M, Hedayati R, Jaberzadeh S. The effects of cerebellar transcranial direct current stimulation on static and dynamic postural stability in older individuals: a randomized double-blind sham-controlled study. Eur J Neurosci 2017;46:75—2884. [22] Yadolahi F, Roostayi MM, Khalkhali-Zavieh M, Rahimi A, Mehrpour M. Modulating neuronal networks to enhance postural control: a review of transcranial direct current stimulation approach. Iran Red Crescent Med J 2019;21:e90337. [23] de Moura MCDS, Hazime FA, Marotti Aparicio LV, Grecco LA, Brunoni AR, Hasue RH. Effects of transcranial direct current stimulation (tDCS) on balance improvement: a systematic review and meta-analysis. Somatosens Motor Res 2019;36:22—135. [24] Woollacott MH, Tang PF. Balance control during walking in the older adult: research and its implications. Phys Ther 1997;77:646—60. [25] Maher CG, Sherrington C, Herbert RD, Moseley AM, Elkins M. Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther 2003;83:713—21. [26] Moseley AM, Herbert RD, Sherrington C, Maher CG. Evidence for physiotherapy practice: a survey of the Physiotherapy Evidence Database (PEDro). Aust J Physiother 2002;48:43—9. [27] de Morton NA. The PEDro scale is a valid measure of the methodological quality of clinical trials: a demographic study. Aust J Physiother 2009;55:129—33. [28] Saruco E, Rienzo FD, Nunez-Nagy S, Rubio-Gonzalez MA, Jackson PL, Collet C, et al. Anodal tDCS over the primary motor cortex improves motor imagery benefits on postural control: a pilot study. Sci Rep 2017;7:480. [29] Yosephi MH, Ehsani F, Zoghi M, Jaberzadeh S. Multi-session anodal tDCS enhances the effects of postural training on balance and postural stability in older adults with high fall risk: primary motor cortex versus cerebellar stimulation. Brain Stimul 2018;11:1239—50. [30] Poortvliet P, Hsieh B, Cresswell A, Au J, Meinzer M. Cerebellar transcranial direct current stimulation improves adaptive postural control. Clin Neurophysiol 2018;129:33—41. [31] Foerster Á, Melo L, Mello M, Castro R, Shirahige L, Rocha S, et al. Cerebellar transcranial direct current stimulation (ctDCS) impairs balance control in healthy individuals. Cerebellum 2017;16:872—5. [32] Ishigaki T, Imai R, Morioka S. Cathodal transcranial direct current stimulation of the posterior parietal cortex reduces steady-state postural stability during the effect of light touch. Neuroreport 2016;27:1050—5. [33] Nomura T, Kirimoto H. Anodal transcranial direct current stimulation over the supplementary motor area improves anticipatory postural adjustments in older adults. Front Hum Neurosci 2018;12:317. [34] Dutta A, Chugh S, Banerjee A, Dutta A. Point-of-care-testing of standing posture with Wii balance board and Microsoft kinect during transcranial direct current stimulation: a feasibility study. Neurorehabilitation 2014;34:789—98. [35] Manor B, Newton E, Abduljalil A, Novak V. The relationship between brain volume and walking outcomes in older adults with and without diabetic peripheral neuropathy. Diabetes Care 2012;35:1907—12.

13 [36] Balasubramaniam R, Wing AM. The dynamics of standing balance. Trends Cogn Sci 2002;6:531—6. [37] Manto M, Bower JM, Conforto AB, Delgado-García JM, da Guarda SNF, Gerwig M, et al. Consensus paper: roles of the cerebellum in motor control—–the diversity of ideas on cerebellar involvement in movement. Cerebellum 2012;11(2):457—87. [38] Lim CY, Shin HI. Noninvasive DC stimulation on neck changes MEP. Neuroreport 2011;22:819—23. [39] Shumway-Cook A, Woollacott MH. Motor control: translating research into clinical practice. Philadelphia: Lippincott Williams & Wilkins; 2012. [40] Demain A, Westby GM, Fernandez-Vidal S, Karachi C, Bonneville F, Do MC, et al. High-level gait and balance disorders in the elderly: a midbrain disease? J Neurol 2014;261:196—206. [41] Mendonca ME, Santana MB, Baptista AF, Datta A, Bikson M, Fregni F, et al. Transcranial DC stimulation in fibromyalgia: optimized cortical target supported by high-resolution computational models. J Pain 2011;12:610—7. [42] Tanaka S, Hanakawa T, Honda M, Watanabe K. Enhancement of pinch force in the lower leg by anodal transcranial direct current stimulation. Exp Brain Res 2009;196:459—65. [43] Ahmed Z. Trans-spinal direct current stimulation modulates motor cortex-induced muscle contraction in mice. J Appl Physiol 2011;110:1414—24. [44] Nitsche M, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 2000;527:633—9. [45] Riberto M, Alfieri FM, de Benedetto Pacheco KM, Leite VD, Kaihami HN, Fregni F, et al. Efficacy of transcranial direct current stimulation coupled with a multidisciplinary rehabilitation program for the treatment of fibromyalgia. Open Rheumatol J 2011;5:45. [46] Winter DA, Patla AE, Rietdyk S, Ishac MG. Ankle muscle stiffness in the control of balance during quiet standing. J Neurophysiol 2001;85:2630—3. [47] Deprez S, Vandenbulcke M, Peeters R, Emsell L, Amant F, Sunaert S. The functional neuroanatomy of multitasking: combining dual tasking with a short-term memory task. Neuropsychologia 2013;51:2251—60. [48] Goble DJ, Coxon JP, Van Impe A, Geurts M, Doumas M, Wenderoth N, et al. Brain activity during ankle proprioceptive stimulation predicts balance performance in young and older adults. J Neurosci 2011;31:16344—52. [49] Sigman M, Dehaene S. Dynamics of the central bottleneck: dual-task and task uncertainty. PLoS Biol 2006;4:e220. [50] Tombu M, Jolicœur P. A central capacity sharing model of dual-task performance. J Exp Psychol Hum Percept Perform 2003;29:3. [51] Filmer HL, Mattingley JB, Dux PE. Improved multitasking following prefrontal tDCS. Cortex 2013;49:2845—52. [52] Truini A, Vergari M, Biasiotta A, Cesa S, Gabriele M, Stefano G, et al. Transcutaneous spinal direct current stimulation inhibits nociceptive spinal pathway conduction and increases pain tolerance in humans. Eur J Pain 2011;15:1023—7. [53] Tsubokawa T, Katayama Y, Yakamato T, Hirayama T, Koyama S. Treatment of thalamic pain by chronic motor cortex stimulation. Pacing Clin Electrophysiol 1991;14:131—4. [54] Celnik P. Understanding and modulating motor learning with cerebellar stimulation. Cerebellum 2015;14:171—4. [55] Nguyen J-P, Nizard J, Keravel Y, Lefaucheur J-P. Invasive brain stimulation for the treatment of neuropathic pain. Nat Rev Neurol 2011;7:699. [56] Priori A, Ciocca M, Parazzini M, Vergari M, Ferrucci R. Transcranial cerebellar direct current stimulation and transcutaneous spinal cord direct current stimulation as innovative tools for neuroscientists. J Physiol 2014;592:3345—69.

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