Effects of blood flow restriction on spine postural control using a robotic platform: A pilot randomized cross-over study

Abstract

BACKGROUND:

Blood flow restriction (BFR) training improves muscle strength and functional outcomes, but the proprioceptive implications of this technique in the rehabilitation field are still unknown.

OBJECTIVE:

The present study aimed at assessing the effects of BFR in terms of stabilometric and balance performance.

METHODS:

In this pilot randomized cross-over study, healthy young adults were included and randomly assigned to Groups A and B. Both groups underwent a postural assessment with and without wearing a BFR device. Study participants of Group A underwent postural baseline assessment wearing BFR and then removed BFR for further evaluations, whereas subjects in Group B performed the baseline assessment without BFR and then with BFR. Stabilometric and balance performance were assessed by the robotic platform Hunova, the Balance Error Scoring System (BESS), the self-reported perceived balance (7-point Likert scale), and discomfort self-rated assessment. Moreover, the safety profile was recorded.

RESULTS:

Fourteen subjects were included and randomly assigned to Group A (n: 7) and Group B (n: 7). Significant differences were shown in balance tests in static conditions performed on the Hunova robot platform in terms of average distance RMS (root-mean-square) with open eyes (OE), anteroposterior (AP) trunk oscillation range with OE, mediolateral (ML) average speed of oscillation with OE, and total excursion AP range with closed eyes (CE) (BFR: 3.44 $\pm$ 1.06; without BFR: 2.75 $\pm$ 0.72; $p=$ 0.041). Moreover, elastic balance test showed differences in Romberg index (BFR: 0.16 $\pm$ 0.16; without BFR: 0.09 $\pm$ 0.07; $p=$ 0.047). No adverse events were reported.

CONCLUSION:

Taken together, our data showed that BFR affects balance performance of healthy subjects. Further studies are needed to better characterize the possible role of BFR treatment in the context of a specific rehabilitation protocol.

Keywords

Blood flow restrictions physiotherapy balance postural assessment rehabilitation

1. Introduction

In the last two decades, a growing literature has been focusing on the potential role of blood flow restriction (BFR) in several physical exercise and rehabilitative programs [1]. BFR is a training technique developed in the 1970s and based on partial arterial occlusion and total venous occlusion achieved through a pneumatic cuff or strap [2]. This technique might be effectively combined with physical exercises, promoting both neuro-muscular adaptations in an anoxic environment and increases in muscle strength and tropism [3, 4, 5]. BFR has been extensively studied in both healthy and post-injured subjects, especially in chronic painful conditions like knee osteoarthritis [6, 7]. Interestingly, growing literature suggests that the main advantage of this technique is the lower training load needed to achieve a hypertrophy response of muscle fibers, with relevant implications for the rehabilitation process of several musculoskeletal conditions [8, 9].

More in detail, the BFR training might improve neuro-muscular strength and hypertrophy in combination with low-intensity exercises (20–40% 1 repetition maximum test-1RM) and functional exercises [1, 10]. At present, the precise mechanisms underpinning these clinical effects still remain unclear. However, it has been proposed that the increase in metabolic stress might shift the recruitment of greater caliber motor units, which are not normally recruited during low-intensity activity [11]. On the other hand, it should be noted that BFR training might have positive effects on pain management, with recent reports suggesting that acute analgesic effects can occur after a single training session with BFR [12, 13, 14, 15]. However, since exercise-induced hypoalgesia can persist up to 24 hours after exercise, it has been hypothesized that pain reduction following BFR training may be related to the same possible mechanisms [13, 16]. In this scenario, the systematic review by Miller et al. [17]showed that BFR training might promote local adaptations at the level of the skeletal muscle system, but limited information is currently available about other systems.

In the rehabilitation field, neuromotor control training is considered a cornerstone of the therapeutic programs tailored for patients affected by motor function impairment. These interventions aim to improve physical performance and neuro-muscular recovery and prevent skeletal muscle injuries. Interestingly, it has been reported that changes in the proprioceptive and motor control functions might increase the prevention of skeletal muscle injuries and increase physical performance in athletes [18, 19]. Similarly, proprioceptive training might be effective in older adults to improve balance control and reduce the risk of falls [20]. Despite several different types of proprioceptive training reported in literature, the effects on proprioceptive outcomes still remain uncertain, probably due to the great heterogeneity of training methods [21].

In this context, posture is defined as the spatial position and orientation of the human body resulting from the neuromuscular activation of skeletal muscle system regulated by the central nervous system based on multisensory inputs [22]. Adequate spine posture is a crucial target of several rehabilitation interventions since optimal results allow for the best athletic gesture and prevention of different musculoskeletal disorders [23]. Although good posture might prevent chronic disabling conditions [24, 25], there is still a gap of knowledge about the optimal strategies affecting spinal posture [22, 26, 27].

Figure 1.

The figure shows the Blood Flow Restriction device and the Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robotic platform used in the study.

Moreover, to the best of our knowledge, the effects of BFR on balance and spinal posture have not been widely explored yet, despite the positive results in terms of strength and muscle mass improvement [1, 10]. Moreover, it should be noted that the impact that BFR on proprioceptive system is still unknown and few studies assessed the effects of proprioceptive training wearing BFR [28].

Therefore, through this pilot randomized cross-over study, we aimed at assessing the effects of BFR on posture and balance and the safety profile in healthy young adults. This could have relevant implications providing clinically useful insights into this novel approach and its possible improvement in the rehabilitation field.

2. Material and methods

2.1 Participants

This study included a series of healthy subjects enrolled between July and December 2022. Inclusion criteria were: a) age between 18 and 40 years old; b) healthy status; c) signing in the informed consent. Exclusion criteria were: a) risk factors for thromboembolism; b) history of venous thrombosis and/or pulmonary embolism; c) risk factors for deep vein thrombosis; d) coagulopathy and/or risk factors for coagulopathies; e) history of peripheral arterial vascular disease or suspected arterial or venous insufficiency of the lower limbs; f) pulse wave velocity (PWV) above 10 m/s [29]; g) anemia; h) trauma to the lower limbs in the previous 30 days; i) physical impairment affecting testing procedures; l) dental surgery in the previous 30 days.

All subjects were assessed for eligibility by a multidisciplinary team composed of an expert physician specialized in physical and rehabilitation medicine and a physiotherapist with years of expertise in postural assessment.

This pilot randomized cross-over study was realized following the CONSORT guidelines [30]. The approval of the trial protocol was obtained from the Ethic Committee of the Azienda Ospedaliera Nazionale SS. Antonio e Biagio e Cesare Arrigo, Alessandria, Italy (ASO.RRF.22.01; protocol number 21982) and was performed in accordance with the Declaration of Helsinki [28] and pertinent national and international regulatory requirements. All researchers involved were instructed to protect the participants’ privacy, and all participants were asked to carefully read and sign an informed consent form and were allowed to revoke their consent to participate in the study without any limitation.

2.2 Intervention

All subjects assessed for eligibility and meeting the eligibility criteria were enrolled in this study. All subjects enrolled were randomly assigned to two groups (Group A or Group B) through a randomization scheme with a 1:1 allocation without blocks. Participants were blinded to group allocation during baseline testing (T0).

•
Group A. All subjects enrolled in Group A wore BFR devices (MAD-UP SAS, 49100 Angers, France) with the blood flow reduction cuffs applied between the proximal third of quadriceps femoris muscle and the inguinal fold. Figure 1 shows the BFR device used in this study. Pressure cuffs were applied by a physical therapist experienced in musculoskeletal disorders and the use of the BFR device. For calibration of the device, the subject lay supine and the pressure cuffs were applied to both limbs targeting the pressure of arterial partial occlusion. The calibration of the pressure was performed automatically by the device, by detecting the initial arterial pressure. The arterial partial occlusion has been subsequently verified by a doppler probe (linear transducer, 7.5–10 MHz, Cerbero, ATL, 20100 Milan, Italy) positioned on the posterior tibial artery. Once the machine has been calibrated, the cuff pressure was adjusted to 80% of occlusal pressure. During the assessments, the device automatically adjusted for blood pressure changes by selecting the program “Performance” in “Free mode” with a blood flow reduction time setting of 10 minutes. After baseline assessments (T1), the subjects removed the BFR device and undergone to the same assessments without BFR device.
•
Group B. Study participants performed all baseline assessments without wearing BFR. After the baseline assessment (T1), all study participants enrolled in Group B performed all stabilometric and balance assessments wearing BFR as previously described in Group A.

Figure 2.

Further details about the study selection and randomization process are summarized in Fig. 2.
2.3 Outcome measures

At the baseline assessment, sociodemographic and anthropometric data were collected. However, due to the intrinsic nature of the study intervention, blinding the operator during the data collection was not possible. Primary and secondary outcomes were assessed at each time point.

The robotic platform Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ (Movendo Technology, Genoa, Italy) was used to assess stabilometric and balance performance through the following balance tests (see Fig. 1 for further details):

•
Balance test in static conditions performed on the Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robot: the platform has been kept fixed for the entire duration of the test. The subject performed the test with both open eyes (OE) and closed eyes (CE) [31];
•
Elastic balance test performed on the Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robot: the subjects were required to remain still on an unstable surface. The platform tilted in response to the displacement of the subject’s body with an elastic, low-load rotational response that opposes the movement induced by the displacement of the subject’s weight. The participant took the test first with open and closed eyes [32]; 1
•
Dynamic balance test performed on the Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robot: the subjects were required to maintain balance on the platform, which performs pre-programmed circular movements with a continuous trajectory (not affected by the movement of the subject). The participant took the test with open and closed eyes [32];

During the Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ assessment, the following stabilometric and balance quantitative measures were considered:

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Sway Area [cm ${}^{2}$ ]: the area of the 95% confidence ellipse of the statokinesigram of the Centre of Pressure (CoP) in the standing static condition as well as the projection of the angular displacement of the platform in the standing dynamic unstable condition. The surface that contains the statokinesigram’s individual points (with a 95% probability) is referred to as the 95% confidence ellipse [33].
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Average distance – RMS [cm]: The average distance, from the center, of the oscillations.
•
Sway Path [cm]: the length of the oscillation path of the CoP trajectory [33].
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Romberg index: Relationship between the stabilometric values with CE and the corresponding values with OE.
•
A-P and M-L Range of oscillation [cm]: Oscillation of the CoP in static conditions or of the platform’s angular displacement projection in unstable dynamic conditions. These variables indicate the amount of oscillation in either the anterior-posterior or mediolateral directions and are related to the subject’s instability [33].
•
A-P and M-L Average speed of oscillation [cm/s]: the average speed of swing in the anteroposterior and mediolateral directions.
•
A-P and M-L Trunk oscillation range [deg]: Parameters that provide information on the compensatory and corrective trunk control strategies required to maintain optimal balance. They were calculated by comparing the maximum and minimum degrees of inclination of the roll (mediolateral range of oscillation, MLO) and pitch (anteroposterior range of oscillation, APO) angles. They are based on the trunk sensor signal (IMU sensor) [33].
•
Trunk movement [deg/s ${}^{2}$ ]: Trunk accelerations measured by the trunk sensor [33].

Secondary outcomes were:

•
Balance Error Scoring System (BESS) score. BESS is a clinical tool for assessing balance and static postural control. The BESS includes three different tasks: double-leg stance, single-leg stance, and tandem stance. Errors are recorded throughout each 20-second trial as the subjects perform the stances with their CE on a firm surface and on a foam surface. Opening eyes, lifting hands off the hips, walking, stumbling, or falling out of position, lifting the forefoot or heel, abducting the hip by more than 30 ${}^{\circ}$ , or failing to return to the test posture in less than five seconds are all considered errors [34].
•
Self-reported perceived balance through 7-point Likert scales: This is a qualitative balance assessment based on self-reported perceived balance based on 7 different items (ranging from “completely stable” to “not at all stable”). The rating was assigned based on the subjective perception of the subject’s own stability.
•
Rating of perceived exertion through Borg scale CR-10: This is a rating scale to assess self-perceived fatigue during the tests. Subjects were asked to give a score from 1 to 10 (1 represents “totally fatigued” and 10 “not at all fatigued”).
•
Discomfort in using the BFR through Numerical Rating Scale (NRS): Subjects were asked to verbally evaluate their discomfort on a scale from 0 to 10 (with 0 equal to “totally comfortable” and 10 equal to “total discomfort”) [35].
•
Safety: Any adverse events that occurred during the tests.

Each session was supervised by the same physiotherapist with a therapist/patient rate of 1:1. All data were analyzed by the same personnel blinded to the treatment performed.
2.4 Statistical analysis

Due to the pilot design of the study, the sample size was not calculated. However, in line with recent recommendations for pilot studies [36], we targeted a sample size of at least 12 study participants.

All data were analyzed using GraphPad Prism 7.0 (GraphPad Software, Inc., San Diego, CA, USA). The non-Gaussian distribution of the outcome variables was assumed due to the low sample size. The Shapiro-Wilk statistic was used to confirm the non-Gaussian distribution of variables. Categorical variables were reported as numbers and ratios, while continuous variables were represented as means $\pm$ standard deviations. A non-Gaussian distribution of variables was considered due to the small sample size assessed. Intra-group differences for each outcome measure were assessed with Wilcoxon’s signed rank test. The between-group analysis was performed with the Mann-Whitney U test comparing experimental intervention to the control intervention. A $p$ -value lower than 0.05 was considered statistically significant. Descriptive statistics were used to summarise the adverse effect of the treatment.

3. Results

Out of 17 subjects assessed for eligibility, 14 young adults met the eligibility criteria and were randomly assigned to Group A (n: 7; mean age: 28.0 $\pm$ 4.20 years; female/male: 3/4) and Group B (n: 7; mean 28.0 $\pm$ 7.04 years; female/male: 3/4). Among the three subjects excluded, 1 subject reported risk factors for thromboembolism and 2 subjects reported traumas to the lower limbs in the past 30 days. Figure 2 shows in detail subjects assessed for eligibility, excluded, and randomized in both groups.

In particular, the subjects in group A were aged 28.0 $\pm$ 4.20 years, with a body mass index (BMI) of 22.94 $\pm$ 3.62 kg/m ${}^{2}$ , whereas the subjects in group B were aged 28.0 $\pm$ 7.04 years, BMI of 24.5 $\pm$ 3.65 kg/m ${}^{2}$ . The between-groups analysis did not show significant differences in terms of age ( $p=$ 0.923), BMI ( $p=$ 0.805), and sex ( $p>$ 0.999). All subjects completed the assessments with and without wearing BFR and no dropouts were registered during the study.

Significant intra-group differences were reported in Group A in balance test performed in static conditions on the Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robot platform in terms of sway area with CE (T0: 5.84 $\pm$ 4.88 cm ${}^{2}$ ; T1: 4.89 $\pm$ 2.54 cm ${}^{2}$ ; $p=$ 0.031) and ML average speed of oscillation with OE. In addition, Group A showed significant changes in terms of ML trunk oscillation range during elastic balance test performed with CE (T0: 5.55 $\pm$ 2.85 deg; T1: 3.56 $\pm$ 1.60 deg; $p=$ 0.031).

Table 1
Clinical outcome measures assessed in the two groups

			Group A (BFR phase)	Group A (Without BFR phase)	$P$ -value	Group B (Without BFR phase)	Group B (BFR phase)	$P$ -value
			$T0$	$T1$		$T0$	$T1$
Balance test	Sway Area [cm2]	OE	2.09 $\pm$ 0.88	1.75 $\pm$ 1.04	0.937	1.45 $\pm$ 0.74	1.79 $\pm$ 0.83	0.297
in static		CE	5.84 $\pm$ 4.88	4.89 $\pm$ 2.54	0.031	5.08 $\pm$ 2.26	5.03 $\pm$ 1.24	0.687
conditions	Average distance	OE	0.48 $\pm$ 0.11	0.44 $\pm$ 0.16	0.437	0.40 $\pm$ 0.10	0.50 $\pm$ 0.15	0.031
	– RMS [cm]	CE	0.76 $\pm$ 0.29	0.72 $\pm$ 0.20	0.500	0.73 $\pm$ 0.20	0.76 $\pm$ 0.09	$>$ 0.999
	Sway Path [cm]	OE	29.66 $\pm$ 6.97	34.84 $\pm$ 9.66	0.156	29.49 $\pm$ 6.15	28.51 $\pm$ 6.23	0.812
		CE	55.34 $\pm$ 11.03	57.48 $\pm$ 13.46	0.687	55.57 $\pm$ 15.07	58.68 $\pm$ 18.61	0.687
	AP COP Range	OE	2.07 $\pm$ 0.60	1.86 $\pm$ 0.76	0.406	1.56 $\pm$ 0.48	1.98 $\pm$ 0.77	0.078
	of oscillation [cm]	CE	3.22 $\pm$ 1.21	2.74 $\pm$ 0.64	0.375	2.77 $\pm$ 0.84	3.66 $\pm$ 0.94	0.078
	ML COP Range	OE	1.57 $\pm$ 0.53	1.45 $\pm$ 0.43	0.469	1.18 $\pm$ 0.34	1.21 $\pm$ 0.29	0.875
	of oscillation [cm]	CE	2.53 $\pm$ 1.00	2.75 $\pm$ 1.00	0.937	2.44 $\pm$ 0.40	2.83 $\pm$ 0.61	0.297
	AP Average speed	OE	0.79 $\pm$ 0.21	0.73 $\pm$ 0.16	0.375	0.73 $\pm$ 0.16	0.77 $\pm$ 0.21	0.469
	of oscillation [cm/s]	CE	1.37 $\pm$ 0.36	1.24 $\pm$ 0.25	0.156	1.23 $\pm$ 0.45	1.50 $\pm$ 0.62	0.531
	ML average speed	OE	0.60 $\pm$ 0.15	0.91 $\pm$ 0.32	0.031	0.65 $\pm$ 0.18	0.56 $\pm$ 0.12	0.297
	of oscillation [cm/s]	CE	1.20 $\pm$ 0.42	1.46 $\pm$ 0.49	0.297	1.37 $\pm$ 0.28	1.23 $\pm$ 0.34	0.687
Romberg index			0.60 $\pm$ 0.62	0.36 $\pm$ 0.12	0.687	0.31 $\pm$ 0.10	0.36 $\pm$ 0.16	0.469
	Trunk movement	OE	0.88 $\pm$ 2.02	0.05 $\pm$ 0.02	0.625	0.06 $\pm$ 0.01	0.07 $\pm$ 0.02	0.500
	[deg/s ${}^{2}]$	CE	0.05 $\pm$ 0.01	0.05 $\pm$ 0.02	0.375	0.06 $\pm$ 0.01	0.05 $\pm$ 0.01	$>$ 0.999
	AP Trunk oscilla-	OE	5.21 $\pm$ 5.02	2.31 $\pm$ 1.11	0.219	1.96 $\pm$ 0.47	3.21 $\pm$ 1.28	0.187
	tion range [deg]	CE	3.14 $\pm$ 1.14	2.17 $\pm$ 1.05	0.437	1.95 $\pm$ 0.84	2.46 $\pm$ 0.46	0.437
	ML Trunk oscilla-	OE	1.29 $\pm$ 0.78	1.22 $\pm$ 0.86	0.312	0.87 $\pm$ 0.39	1.18 $\pm$ 0.43	0.187
	tion range [deg]	CE	1.34 $\pm$ 0.31	1.23 $\pm$ 0.77	0.687	0.97 $\pm$ 0.29	1.28 $\pm$ 0.63	0.437
Elastic	Sway Area [cm ${}^{2}]$	OE	22.99 $\pm$ 21.25	29.43 $\pm$ 46.97	0.937	15.01 $\pm$ 17.32	33.09 $\pm$ 51.91	0.156
balance test		CE	193.99 $\pm$ 127.32	219.00 $\pm$ 246.56	0.812	149.31 $\pm$ 106.82	166.47 $\pm$ 137.36	0.687
	Average distance –	OE	1.57 $\pm$ 0.69	1.67 $\pm$ 1.09	$>$ 0.999	1.27 $\pm$ 0.74	1.66 $\pm$ 1.34	0.297
	RMS [cm]	CE	4.51 $\pm$ 1.45	4.56 $\pm$ 2.28	0.812	3.89 $\pm$ 1.64	4.02 $\pm$ 1.85	0.844
	Sway Path [cm]	OE	68.46 $\pm$ 31.85	63.05 $\pm$ 44.25	0.297	59.78 $\pm$ 42.30	60.62 $\pm$ 50.83	0.937
		CE	226.22 $\pm$ 72.36	254.35 $\pm$ 108.71	0.812	237.77 $\pm$ 89.01	243.39 $\pm$ 101.79	0.937
	AP COP Range of	OE	6.44 $\pm$ 2.52	7.02 $\pm$ 4.26	0.812	5.19 $\pm$ 3.20	6.46 $\pm$ 5.48	0.687
	oscillation [cm]	CE	17.90 $\pm$ 4.43	18.85 $\pm$ 7.13	0.687	15.48 $\pm$ 6.66	15.62 $\pm$ 6.92	0.937
	ML COP Range of	OE	3.69 $\pm$ 2.75	3.91 $\pm$ 3.77	$>$ 0.999	2.76 $\pm$ 1.95	3.67 $\pm$ 4.00	0.812
	oscillation [cm]	CE	14.74 $\pm$ 5.83	13.79 $\pm$ 8.05	0.812	11.91 $\pm$ 4.81	11.81 $\pm$ 6.44	0.937
	AP Average speed	OE	2.14 $\pm$ 0.92	1.91 $\pm$ 1.24	0.219	1.95 $\pm$ 1.37	1.85 $\pm$ 1.40	0.687
	of oscillation [cm/s]	CE	6.44 $\pm$ 2.03	7.21 $\pm$ 3.10	0.687	6.80 $\pm$ 2.60	6.96 $\pm$ 2.81	0.937
	ML Average speed	OE	0.80 $\pm$ 0.63	0.80 $\pm$ 0.88	0.937	0.58 $\pm$ 0.55	0.79 $\pm$ 0.98	0.469
	of oscillation [cm/s]	CE	3.74 $\pm$ 1.63	4.30 $\pm$ 1.91	0.937	3.92 $\pm$ 1.56	4.06 $\pm$ 2.06	0.937
Romberg index			0.16 $\pm$ 0.19	0.11 $\pm$ 0.08	0.453	0.08 $\pm$ 0.05	0.16 $\pm$ 0.14	0.094
	Trunk movement	OE	0.07 $\pm$ 0.03	0.06 $\pm$ 0.02	0.937	0.07 $\pm$ 0.01	0.07 $\pm$ 0.03	0.375
	[deg/s ${}^{2}]$	CE	0.13 $\pm$ 0.07	0.12 $\pm$ 0.04	0.453	0.13 $\pm$ 0.04	0.12 $\pm$ 0.03	0.469
	AP Trunk oscillation	OE	5.10 $\pm$ 6.09	3.14 $\pm$ 1.97	0.375	2.96 $\pm$ 1.16	5.49 $\pm$ 6.51	0.687
	range [deg]	CE	6.83 $\pm$ 4.85	5.48 $\pm$ 3.90	0.469	6.63 $\pm$ 3.11	5.72 $\pm$ 2.76	0.578
	ML Trunk oscilla-	OE	4.16 $\pm$ 6.80	1.71 $\pm$ 1.55	0.125	1.46 $\pm$ 0.78	2.03 $\pm$ 2.06	0.937
	tion range [deg]	CE	5.55 $\pm$ 2.85	3.56 $\pm$ 1.60	0.031	4.20 $\pm$ 2.12	4.72 $\pm$ 4.37	0.812
Dynamic	Trunk movement	OE	0.10 $\pm$ 0.04	0.08 $\pm$ 0.03	0.750	0.09 $\pm$ 0.01	0.09 $\pm$ 0.02	0.625
balance test	[deg/s ${}^{2}]$	CE	0.13 $\pm$ 0.04	0.10 $\pm$ 0.02	0.375	0.14 $\pm$ 0.11	0.10 $\pm$ 0.03	0.125
	AP Trunk oscillation	OE	7.16 $\pm$ 5.08	6.34 $\pm$ 5.17	0.625	5.03 $\pm$ 1.42	6.21 $\pm$ 2.17	0.578
	range [deg]	CE	6.92 $\pm$ 1.74	5.22 $\pm$ 1.16	0.312	6.44 $\pm$ 1.13	5.29 $\pm$ 1.82	0.219
	ML Trunk oscilla-	OE	3.03 $\pm$ 1.46	4.49 $\pm$ 2.29	0.625	3.72 $\pm$ 1.68	3.59 $\pm$ 1.65	0.578
	tion range [deg]	CE	5.00 $\pm$ 1.35	3.86 $\pm$ 0.81	0.312	3.63 $\pm$ 1.49	3.69 $\pm$ 1.05	0.812
BESS	Firm surface	Double-leg stance	0	0	$>$ 0.999	0	0	$>$ 0.999
		Single-leg stance	5.40 $\pm$ 0.55	4.60 $\pm$ 0.89	0.250	3.00 $\pm$ 2.83	2.50 $\pm$ 3.21	0.875
		Tandem stance	0.80 $\pm$ 0.84	0.40 $\pm$ 0.55	0.625	0.50 $\pm$ 1.22	0.17 $\pm$ 0.41	$>$ 0.999

Table 1, continued
			Group A (BFR phase)	Group A (Without BFR phase)	$P$ -value	Group B (Without BFR phase)	Group B (BFR phase)	$P$ -value
			$T0$	$T1$		$T0$	$T1$
	Foam surface	Double-leg stance	0	0	$>$ 0.999	0	0	$>$ 0.999
		Single-leg stance	8.40 $\pm$ 1.82	7.40 $\pm$ 1.82	0.375	7.17 $\pm$ 3.37	6.17 $\pm$ 1.17	0.875
		Tandem stance	5.00 $\pm$ 3.39	3.80 $\pm$ 3.27	0.562	2.33 $\pm$ 2.07	1.50 $\pm$ 1.76	0.437
Likert scale	Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$		5.20 $\pm$ 0.45	5.00 $\pm$ 1.22		6.33 $\pm$ 0.82	5.33 $\pm$ 0.82	/
balance perceived	BESS		4.20 $\pm$ 1.30	4.40 $\pm$ 1.34		5.67 $\pm$ 1.03	4.67 $\pm$ 0.82	/
Rating perceived exerction	Borg scale CR-10		3.20 $\pm$ 1.48	/	/	/	3.50 $\pm$ 1.97	/
Discomfort	NRS		1.80 $\pm$ 3.03	/	/	/	4.17 $\pm$ 2.40	/
Safety	Number of adverse events occurred		0	0	$>$ 0.999	0	0	$>$ 0.999

Continuous variables are expressed as means $\pm$ standard deviations. Significant results ( $p<$ 0.05) are in bold. Abbreviations: AP: anteroposterior; BESS: Balance Error Scoring System; CE: Closed Eyes; COP: Center of Pressure; ML: mediolateral; NRS: Numerical Rating Scale; OE: Open Eyes; T0: baseline assessment; T1: after baseline assessment.

In contrast, the intra-group statistical analysis in Group B showed significant effects in balance test in static conditions on the Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robot platform in terms of average distance of RMS with OE (T0: 0.40 $\pm$ 0.10 cm; T1 0.50 $\pm$ 0.15 cm; $p=$ 0.031). The Table 1 shows the results of the intragroup analysis for the outcome measures.

Table 2

Results of the pooled analysis for the outcome measures

			Without BFR	BFR	$P$ -value
Balance test in static	Sway Area [cm2]	OE	2,89 $\pm$ 2,47	3,40 $\pm$ 3,92	0,391
conditions		CE	3.69 $\pm$ 2.41	3.96 $\pm$ 1.89	0.463
	Average distance – RMS [cm]	OE	0.42 $\pm$ 0.13	0.49 $\pm$ 0.13	0.019
		CE	0.73 $\pm$ 0.15	0.76 $\pm$ 0.2	0.381
	Sway Path [cm]	OE	32.16 $\pm$ 8.26	29.09 $\pm$ 6.38	0.241
		CE	56.53 $\pm$ 13.76	57.01 $\pm$ 14.8	$>$ 0.999
	AP COP Range of oscillation [cm]	OE	1.71 $\pm$ 0.63	2.03 $\pm$ 0.67	0.051
		CE	2.75 $\pm$ 0.72	3.44 $\pm$ 1.06	0.041
	ML COP Range of oscillation [cm]	OE	1.32 $\pm$ 0.4	1.39 $\pm$ 0.45	0.521
		CE	2.59 $\pm$ 0.75	2.68 $\pm$ 0.82	0.426
	AP Average speed of oscillation [cm/s]	OE	0.73 $\pm$ 0.15	0.78 $\pm$ 0.2	0.235
		CE	1.23 $\pm$ 0.35	1.43 $\pm$ 0.49	0.111
	ML Average speed of oscillation [cm/s]	OE	0.78 $\pm$ 0.28	0.58 $\pm$ 0.13	0.012
		CE	1.41 $\pm$ 0.38	1.21 $\pm$ 0.37	0.222
	Romberg index		0.33 $\pm$ 0.11	0.48 $\pm$ 0.45	0.365
	Trunk movement [deg/s ${}^{2}]$	OE	0.05 $\pm$ 0.02	0.44 $\pm$ 1.37	0.21
		CE	0,05 $\pm$ 0,01	0,05 $\pm$ 0,01	0.562
	AP Trunk oscillation range [deg]	OE	2.16 $\pm$ 0.89	4.13 $\pm$ 3.52	0.042
		CE	2,08 $\pm$ 0.93	2.780 $\pm$ 0.98	0.147
	ML Trunk oscillation range [deg]	OE	5.69 $\pm$ 15.86	1.23 $\pm$ 0.59	0.965
		CE	1.12 $\pm$ 0.61	1.3 $\pm$ 0.49	0.831
Elastic balance test	Sway Area [cm ${}^{2}]$	OE	13.62 $\pm$ 13.86	28.04 $\pm$ 38.47	0.08
		CE	184.62 $\pm$ 186.1	180.23 $\pm$ 128.04	0.501
	Average distance – RMS [cm]	OE	1.47 $\pm$ 0.92	1.61 $\pm$ 1.03	0.391
		CE	4.22 $\pm$ 1.94	4.26 $\pm$ 1.61	0.593
	Sway Path [cm]	OE	61.42 $\pm$ 41.62	64.54 $\pm$ 40.95	0.426
		CE	246.06 $\pm$ 95.84	234.81 $\pm$ 85.31	0.807
	AP COP Range of oscillation [cm]	OE	6.11 $\pm$ 3.74	6.45 $\pm$ 4.1	0.541
		CE	17.17 $\pm$ 6.85	16.76 $\pm$ 5.71	0.903
	ML COP Range of oscillation [cm]	OE	3.33 $\pm$ 2.94	3.68 $\pm$ 3.3	0.855
		CE	12.85 $\pm$ 6.45	13.28 $\pm$ 6.1	0.625
	AP Average speed of oscillation [cm/s]	OE	1.93 $\pm$ 1.26	1.99 $\pm$ 1.15	0.625
		CE	7.01 $\pm$ 2.76	6.7 $\pm$ 2.37	0.819
	ML Average speed of oscillation [cm/s]	OE	0.69 $\pm$ 0.71	0.8 $\pm$ 0.79	0.703
		CE	4.11 $\pm$ 1.69	3.9 $\pm$ 1.79	$>$ 0.999
	Romberg index		0.09 $\pm$ 0.07	0.16 $\pm$ 0.16	0.047
Dynamic balance test	Trunk movement [deg/s ${}^{2}]$	OE	0.08 $\pm$ 0.02	0.09 $\pm$ 0.03	0.312
		CE	0.12 $\pm$ 0.08	0.11 $\pm$ 0.04	0.668
	AP Trunk oscillation range [deg]	OE	5.61 $\pm$ 3.35	6.61 $\pm$ 3.49	0.38
		CE	5.93 $\pm$ 1.26	5.97 $\pm$ 1.9	0.85
	ML Trunk oscillation range [deg]	OE	4.04 $\pm$ 1.9	3.36 $\pm$ 1.53	0.38
		CE	3.73 $\pm$ 1.21	4.24 $\pm$ 1.31	0.266
BESS	Firm surface	Double-leg stance	0	0	$>$ 0.999
		Single-leg stance	3.73 $\pm$ 2.24	3.82 $\pm$ 2.75	0.453
		Tandem stance	0.45 $\pm$ 0.93	0.45 $\pm$ 0.69	0.687
	Foam surface	Double-leg stance	0	0	$>$ 0.999
		Single-leg stance	7.27 $\pm$ 2.65	7.18 $\pm$ 1.83	0.695
		Tandem stance	3.0 $\pm$ 2.65	3.09 $\pm$ 3.08	0.734
Likert scale balance	Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$		5.73 $\pm$ 1.19	5.27 $\pm$ 0.65	0.398
perceived	BESS		5.09 $\pm$ 1.3	4.45 $\pm$ 1.04	0.062
Rating perceived exerction	Borg scale CR-10		/	3.36 $\pm$ 1.69	/
Discomfort	NRS		/	3.09 $\pm$ 2.84	/
Safety	Number of adverse events occurred		0	0	$>$ 0.999

The between-groups analysis compared showed significant differences ( $p<$ 0.05) in the balance tests in static conditions performed on the Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robot platform. More in detail, the between-group analysis showed significant differences in terms of average distance RMS with OE (BFR: 0.49 $\pm$ 0.13 cm; without BFR: 0.42 $\pm$ 0.13 cm; $p=$ 0.019) and total excursion AP range with CE (BFR: 3.44 $\pm$ 1.06; without BFR: 2.75 $\pm$ 0.72; $p=$ 0.041). Moreover, significant differences were found in terms of both AP trunk oscillation range (BFR: 4.13 $\pm$ 3.52 deg; without BFR: 2.16 $\pm$ 0.89 deg; $p=$ 0.042) and ML average speed of oscillation with OE (BFR: 0.58 $\pm$ 0.13 cm/s, without BFR: 0.78 $\pm$ 0.28 cm/s; $p=$ 0.012). No significant differences were reported for the other outcome measures of the balance test in static conditions on the Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robot platform. Table 2 shows further details about the balance tests in static conditions.

The assessment in the elastic balance test performed on the Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robot showed significant between-group differences in terms of Romberg index (BFR: 0.16 $\pm$ 0.16; without BFR: 0.09 $\pm$ 0.07; $p=$ 0.047). No significant differences were reported for the other outcomes assessed with the elastic balance test.

Lastly, there were no significant differences in the outcome measures assessed with dynamic balance test on the Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robot platform, BESS test, and Likert scale balance perceived. Further details about the between-group analysis are shown in detail in Table 2.

All subjects included showed no side effects. The discomfort during the BFR test was registered by NRS scale, showing a mean of 3.08 $\pm$ 2.84.

4. Discussion

In recent years, BFR has been introduced in the rehabilitation management of different chronic disabling conditions to reduce pain intensity, weight load, and improving anabolic changes in trained muscles [1]. Despite several reports focused on the positive impact of BFR training in terms of muscle strength and functional performance [37, 38, 39], the effects on balance performance and spinal posture have not been characterized yet.

In light of this consideration, this pilot randomized crossover study aimed at assessing the postural changes induced by BFR device, in order to provide clinically relevant evidence about the effects on neuromuscular control during rehabilitation wearing BFR.

Interestingly, our results showed that BFR might affect balance performance in both static and dynamic conditions. More in detail, our results showed that BFR might interact with AP average distance, AP trunk oscillation range, and ML average speed of oscillation in static conditions with OE. Interestingly, the recent study by Burkhardt et al. [28] assessed the effects of BFR on muscle activation during dynamic balance exercises. The authors reported that wearing BFR might affect the activation of vastus lateralis and soleus muscles and significant effects of BFR were reported in terms of perceived postural instability [28]. However, there are no previous studies assessing the effects of BFR in terms of static balance performance, elastic balance performance, and dynamic balance performance. On the other hand, dynamic balance exercise combined with BFR might be an option to potentially improve benefits of proprioceptive training, especially considering the increasing evidence suggesting that BFR might be most beneficial combined with low-intensity muscle training [40]. In this context, dynamic balance training is commonly performed with low-intensity muscle contraction (20–40% 1RM) and might take potential advantages of BFR integration without adjusting exercise intensity.

Moreover, it was interesting to notice that our data underlined significant differences in Romberg index during elastic balance test on the Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robotic platform. Romberg index might indirectly quantify the effects of visual sensation deprivation in stabilometric performance, leading to assessing vestibular and somatosensory compensation in balance control [41, 42]. Thus, the between groups differences in Romberg index might be partly explained by the peripheral effects of BFR. More in detail, muscular activation and muscular response might be crucially affected by BFR with several reports emphasizing that postural muscles are mainly composed of a high percentage of type I muscle fibers characterized by aerobic metabolism [43, 44, 45].

Therefore, BFR might affect the muscle response due to the limitation of oxygen delivery resulting in different expressions of muscle force in proprioceptive training [46, 47]. In contrast, growing literature is now suggesting that BFR might affect peripheral sensation during exercise training, reducing pain intensity [48, 49]. Despite the antinociceptive role of BFR has not been fully characterized, BFR might affect the afferent signal of pain sensation by an anaerobic environment. In this context, hypoxic conditions might modulate pain intensity through a noxious conditioning stimulation mechanism. More in detail, an ascending painful input from a distant body area (or conditioning stimulus) reduces the perception of another painful input from other sites of the body. As result, BFR could be considered a conditioning stimulation modulating ascending inputs of pain sensation [50].

On the other hand, BFR might affect not only pain sensation but also other multisensory peripheral inputs with previous reports reporting secondary effects of BFR training including paraesthesia [48]. Interestingly, these sensitive peripheral alterations might include proprioceptive inputs in accordance with the significant results found in terms of Romberg index during elastic test on the Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robotic platform. Thus, BFR might alter peripheral proprioceptive signal that might be compensated by visual sensation in balance test, but it might result in impairment in balance performance with CE.

Although BFR might affect balance performance, the subjects included did not report differences in terms of subjective balance perceived (with BFR: 5.73 $\pm$ 1.19; without BFR: 5.27 $\pm$ 0.65; p: 0.398), in contrast with a previous study in literature [28]. Thus, operators should be aware that potential alterations in balance stability during proprioceptive training wearing BFR might be not perceived by the subjects. On the other hand, no adverse events were registered wearing BFR and discomfort rate of this tool were low (NRS: 3.08 $\pm$ 2.84), supporting the potential integration of this BFR device in proprioceptive exercise training, even combined with other robotic technologies. Vascular comorbidities and related risk factors should always be thoroughly examined prior to the BFR training by the specialist. In addition, the optimal percentage of arterial occlusion is still debated in literature (ranging from 40% to 80%), and regulation requires a specialized professional, hence self-application is still suboptimal [51, 52].

To the best of our knowledge, this is the first study combining robotic rehabilitation technology with BFR. In recent years, growing attention is rising on digital innovation and robotic rehabilitation for several disabling disorders [53, 54, 55]. In this scenario, several studies have assessed stabilometric performance with Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robotic platform, reporting that Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ might be considered a promising robotic tool to assess multidimensional balance parameters [33, 56, 57]. Interestingly, our data suggested that Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robotic training might be effectively integrated with other clinical tools currently used in clinical settings, including BFR.

However, we are aware that this study is not free from limitations. Firstly, the small sample size severely limits the strength of our findings. On the other hand, it should be noted that, according to the pilot design, we targeted a specific sample size following the most recent recommendations for pilot studies [36]. In addition, compared with a parallel group design, less participants are required for a cross-over study to obtain the same power for a target effect size according to the CONSORT statement [58].

Moreover, healthy subjects might be characterized by a high endocrine system with potential implications of these results in terms of applicability for pathological subjects. However, were considered healthy subjects in accordance with the phase I trial recommendations of the US Food and Drug [59] since no previous study assessed the neurophysiological implications of BFR in balance control in humans.

In this context, PWV, which represents an independent risk factor for cardiovascular accidents, was assessed as inclusion criteria, but it was not assessed at T1. PWV reflects arterial stiffness, and an increase of 1.0 m/s in PWV leads to a 12–14% increased risk of cardiovascular events [60]; it is known that strength training increases in healthy young people the arterial stiffness [60], but it is not known if BFR training may induce a greater risk. A recent systematic review on low-intensity resistance exercise with moderate BFR reported that BFR applied to the lower limbs may induce positive effects related to arterial stiffness, although a degree of caution has been suggested in order to prevent unwanted responses in arterial stiffness markers [61].

Another major limitation is that the study participants did not perform specific training to the BFR device and Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robotic platform before the balance assessments. On the other hand, a randomized cross-over design allows balancing any confounders in the between-group analysis reducing implications of any differences in subjects’ characteristics including potential tail effects of BFR, and hormone or endocrine response due to gender differences or menstruation period in women participants.

Lastly, a superficial electromyography assessment might further characterize the neuromuscular control impairment from a physiological perspective. Despite these considerations, it has been already assessed in literature the effect of BFR on muscle activation outcomes [28, 62], although no previous study assessed balance performance with objective stabilometric assessment during BFR training.

5. Conclusions

In this pilot cross-over study, we assessed the effects of BFR on balance performance and safety profile in healthy adults randomly assigned to two groups. Taken together, our findings suggested a potential positive effect of BFR in static and elastic balance performance on the Hunova ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}\textregistered}$ robotic platform. However, subjects included did not report differences in terms of subjective balance perceived. This could have intriguing implications to improve proprioceptive training in the rehabilitation field. Albeit the biological mechanisms underpinning the effects of BFR are still far from being fully understood, to the best of our knowledge, this is the first study assessing the impact of BFR on balance performance using a robotic platform. However, further studies assessing larger samples of patients with impaired balance performance are needed to better characterize the role of BFR on balance training and its potential integration in a tailored rehabilitation approach.

Funding

This study is part of the project NODES which received funding from the MUR – M4C2 1.5 of PNRR (grant agreement no. ECS00000036).

Ethics statement

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethic Committee of the Azienda Ospedaliera Nazionale SS. Antonio e Biagio e Cesare Arrigo, Alessandria, Italy (ASO.RRF.22.01; protocol number: 21982). Informed consent was obtained from all individual participants included in the study.

Footnotes

Acknowledgments

The authors would like to thank Stefano Moalli and Giulia Stacchino for their support of this work.

Conflict of interest

None to report.

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Effects of blood flow restriction on spine postural control using a robotic platform: A pilot randomized cross-over study

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1. Introduction

2.1 Participants

2.2 Intervention

3. Results

Table 1 Clinical outcome measures assessed in the two groups

5. Conclusions

Funding

Ethics statement

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Clinical outcome measures assessed in the two groups