Effects of Neuromuscular Training on Physical Performance in Older People: A Systematic Review

This systematic review aimed to assess the available evidence on the effects of neuromuscular training on physical performance in older adults. A literature search was conducted across four databases (Psychology and Behavioral (EBSCO), Scopus, Web of Science and PubMed). The PRISMA guidelines were followed. The PEDro scale and Cochrane risk of bias tool were used to assess the quality of and risk of bias in the studies, respectively. The protocol was registered in PROSPERO (code: CRD42022319239). The outcomes were muscle strength, cardiorespiratory fitness, postural balance and gait speed. From 610 records initially found, 10 were finally included in the systematic review, involving 354 older people with a mean age of 67.3 years. Nine of them reported significant changes in at least one variable related to physical performance in the intervention compared to the control groups. The neuromuscular training caused significant improvements in postural balance, flexibility, cardiorespiratory fitness, strength power of the upper and lower limbs and autonomy. The available evidence indicates that neuromuscular training has a positive effect on some variables of physical performance, especially in postural balance; however, the methodological quality and certainty of the evidence in the available literature are limited. Therefore, a greater number of high-quality studies are required to draw definitive conclusions.


Introduction
Aging is linked to anatomical and physiological changes capable of inducing a deterioration in functionality and autonomy [1,2]. Among the changes that occur with age, those that affect the musculoskeletal, cardiovascular and somatosensory systems (visual, vestibular and proprioception) are highly prevalent [1]. This causes changes in the ability to maintain posture, gait and the capacity to carry out daily tasks independently [3]. In addition to an increase in muscle weakness, fatigue and functional deterioration, the existing Life 2023, 13, 869 2 of 14 evidence has also suggested that aging is linked to a deterioration of proprioception and the vestibular system, resulting in a poor perception of the position of the body in space, which causes alterations in postural balance, a greater probability of falls and impaired physical performance [4,5].
Physical performance is the capacity to perform daily activities with vigor, without undue fatigue, and with enough energy to take part in leisure activities and handle unexpected emergencies [6,7]. Currently, it is considered a multidimensional concept, operationalized as a set of measurable attributes or components related to health and abilities, including muscular strength, cardiorespiratory fitness, flexibility, postural balance, agility (dynamic postural balance) and gait speed [8]. It has been reported that physical performance is strongly related to health status across the lifespan; however, declines in physical performance can also differ within individuals and therefore relate to healthy aging [8,9].
Various physical exercise programs have been recommended to attenuate the loss of muscle strength and the deterioration of physical performance caused by aging [10][11][12]. For the most part, traditional exercise programs for the elderly are based on interventions with strength training, cardiorespiratory training, combined exercise (cardiorespiratory and strength) and multicomponent programs (cardiorespiratory, strength, flexibility and postural balance) [13,14]. However, the evidence for emerging rehabilitation programs, such as neuromuscular training, is limited, especially in older adults [15,16].
Currently, in comprehensive physical rehabilitation programs, the combination of proprioceptive, strength, and postural balance exercises is known as neuromuscular training [17]. Neuromuscular training is based on the adequate stimulation of peripheral receptors (i.e., mechanoreceptors) in order to improve the integration of muscular responses [18]. According to the literature, neuromuscular training can enhance unconscious motor responses by optimizing afferent signals and the integration of information at the level of the cerebral cortex, favoring dynamic control of the joints [19]. Recently, neuromuscular training programs have been developed in people with knee and hip osteoarthritis (OA) [20,21], in addition to interventions aimed at improving postural balance and the risk of falls in older people. However, the literature is still limited when reporting the benefits that neuromuscular training can generate on physical performance. For this reason, the aim of this systematic review was to analyse scientific articles related to the effects of neuromuscular training on physical performance in older people.

Protocol and Registration
This systematic review was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [22]. The protocol was registered and approved by PROSPERO (CRD42022319239).

Eligibility Criteria
For this systematic review, the inclusion criteria were as follows: (i) randomized controlled trials (RCT) or quasi-experimental clinical trials that use neuromuscular training as an intervention in older people of both sexes.
As the age definitions for "older people" vary around the world, people over 60 years of age were chosen to enable a broad worldwide inclusion. The exclusion criteria were: (i) cross-sectional, retrospective and prospective studies, or whose interventions were not centered on neuromuscular training; (ii) non-original articles (e.g., translations, book reviews, letters to the editor); (iii) duplicate articles; (iv) review articles (e.g., narrative reviews, systematic reviews, meta-analyses); and (v) case studies. Additionally, the studies were incorporated into the systematic review using the PICOs framework (population, intervention, comparator, outcomes and study design).

Information and Database Search Process
The search process was performed between May and July 2022, using four databases: Psychology and Behavioral (EBSCO), Scopus, Web of Science and PubMed. Original articles without language restrictions and published in the last 60 years (January 1950 to the date of extraction April 2022) were included. The search string used was the following: ("neuromuscular training" OR "proprioceptive training program" OR "sensorimotor training program") AND ("physical performance" OR "physical fitness" OR "functional fitness" OR "functional capacity" OR "functionality" OR "performance" OR "strength" OR "resistance" OR "endurance" OR "cardiorespiratory fitness" OR "balance" OR "stability" OR "agility" OR "postural control" OR "gait" OR "speed" OR "locomotion" OR "SPPB") AND ("old people" OR "elders" OR "senior" OR "old adult" OR "aged" OR "older people" OR "older adults" OR "geriatric").

Studies Selection and Data Collection Process
The research was transferred to the EndNote references manager (version X8.2, Clarivate Analytics, Philadelphia, PA, USA). The searching, removing duplicates, screening titles and abstracts, and examining full texts were performed by two independent authors (YCC and EGM). At this point, no discrepancies were discovered. The full text of all the potentially eligible studies was reviewed, and the reasons for excluding those studies that did not meet the selection criteria were reported.

Methodological Quality Assessment and Risk of Bias
The selected studies were evaluated through the PEDro scale. This scale evaluates the methodological quality of the studies, considering 11 points that include the blinding procedure, statistical analysis, information on randomization and the presentation of the results in the evaluated research [23]. Criterion 1 assesses the external validity and is not included in the result. From criteria 2 to 11, the internal validity of the article was evaluated with a standardized scoring system (range from 0 to 10). The study quality was classified as excellent (9-10 points), good (6-8 points), fair (4-5 points) and poor (<4 points) [24]. This process was conducted independently by two authors (YCC and EGM).
Using Review Manager 5.3 software, two independent authors (YCC and EGM) evaluated the risk of bias in the included trials (Cochrane Collaboration, Oxford, UK), and differences concerning the methodological quality were resolved by discussion. The Cochrane criteria were used to assess the risk of bias, and selection bias, performance bias, detection bias, attrition bias, reporting bias and other potential biases were considered. The risk of bias was categorized into three grades: low risk, high risk and some concerns [25].

Data Synthesis
The following information was obtained and examined from the selected studies: (i) authors and publication year; (ii) the country where the research was carried out; (iii) the study design; (iv) the sample's initial health condition; (v) the number of participants in the intervention and control groups, and percentage of women; (vi) the mean age of the sample; (vii) the activities developed in the experimental groups (EG) and control groups (CG), the training volume (total duration, weekly frequency and time per session); (viii) the data collection instruments of physical performance; and (ix) the main outcomes of the studies.

Studies Selection
In the study identification phase, 610 articles were found. Then, the duplicates were removed (n = 493), and the studies were filtered by selecting the title, abstract, and keywords, obtaining 117 references. In the analysis phase, two studies were excluded because the full text was not accessed. Forty-three studies were analysed in the full text, four of which were excluded due to not being neuromuscular training; 13 because the mean age of the participants was less than 60 years; 3 for not having physical performance assessments;  8 for not having a control group and 5 for being case studies or reviews. After this process, 10 studies in total met all the requirements for selection ( Figure 1) [26][27][28][29][30][31][32][33][34][35].

Risk of Bias
The details about the risk of bias in the included studies are shown in Figure 2A,B. Five studies presented a high risk of selection bias, as they used single-blinded assessments and did not perform adequate randomization, while five were categorized as "some concerns".

Risk of Bias
The details about the risk of bias in the included studies are shown in Figure 2A, B. Five studies presented a high risk of selection bias, as they used single-blinded assessments and did not perform adequate randomization, while five were categorized as "some concerns".  [26,27,28,29,30,31,32,33,34,35]; (B) risk of bias summary. Table 2 summarizes the variables analyzed in each of the selected studies. Of these, two were performed in South America [28,32], five in Europe [29][30][31]33,34], two in Asia [26,35] and one in Africa [27]. Concerning the design of the studies, eight were randomized controlled trials, and two were quasi-experimental clinical trials.  Table 2 summarizes the variables analyzed in each of the selected studies. Of these, two were performed in South America [28,32], five in Europe [29][30][31]33,34], two in Asia [26,35] and one in Africa [27]. Concerning the design of the studies, eight were randomized controlled trials, and two were quasi-experimental clinical trials.

Physical Performance Outcomes and Collection Instruments
Muscle strength was assessed by two studies [32,35]. The first assessed upper and lower limb strength through functional tests included in the Senior Fitness Test battery [32], while the second study measured lower limb muscle strength with the climbing-up-anddown-stairs test [35].
Cardiorespiratory fitness was analysed by one of the studies using the six-minute walk test [32]. For its part, the flexibility of the lower and upper limbs was assessed using the Sit and Reach and Back Scratch Tests, respectively [32].
Six studies evaluated postural balance through the use of the Biodex Stability System (BBS) [27,30] or force platforms [26,31,33,34]  Step Test, a test where the person was required to step sequentially over four rods arranged in a cross on the ground [29].
Finally, three studies included the evaluation of gait speed, for which they used a 10 m walk test [32] and a 60 m walk test [30,35].
The neuromuscular training carried out in the studies included proprioceptive, strength and postural balance exercises. Of the 10 studies selected, eight maintained the classic structure of a training session, including a warm-up, development (where neuromuscular activities were performed) and a cool-down; however, not all reported all the activities performed and/or the training volume [27,28,[31][32][33]35]. Table 3 summarizes the neuromuscular training protocols used by the studies. Five studies included proprioceptive exercises that were progressive in intensity, beginning with simpler activities such as (a) standing upright on a firm surface and then on a soft surface; and (b) a one-legged stance with eyes open and closed on a firm surface and then on a soft surface [26][27][28]30,34]. More complex functional activities were also incorporated, such as: (a) walking on a firm surface and then on a foam surface; (b) squat or postural balance exercise on a wobble board [27,28,34]. Agility was also part of the intervention, including walking activities in different directions [28]. The routines included activities aimed at developing coordination, speed and muscle power, as well as multi-articular exercises for the upper and lower limbs [32,33]. Among the materials used for the execution of the activities were firm mats (yoga mats), soft mats, oscillating tables, air pillows and cones [32], in addition to softballs, tennis balls, rubber bands [27], BOSU balls [31] and a suspension system [35].  Table 3. Neuromuscular training protocol.

Neuromuscular Training
Ahmad et al., 2019 [26] Warm-up: used cycle ergometer or treadmill at the intensity of 50% to 60% HRmax (10 min). Developing: wall slides, core exercises, balance exercises on an unstable surface, and gait training (different patterns of walking) (50 to 60 min). Cool-down: included deep breathing, abdominal breathing and mild stretching (10 min).
Ahmed, 2011 [27] Consisted of three stages: static, dynamic and functional (30 min). Warm-up: joint mobility. Developing: intermittent activities organized in a circuit that required agility, coordination, velocity and muscle power of a set of complex motor systems. In addition, they included multi-articular exercises for lower and upper limbs with intense activation of stabilizing muscles of the spine, organized in a circuit and intermittent high-intensity activities (60 min). Cool-down was not reported.
Rezaeipour & Apanasenko, 2020 [33] Warm-up: shuttle run, backward running, five stretching techniques for the trunk and lower extremities, two strengthening exercises, two impact-training techniques, such as box jumps, as well as doing two-leg versus one-leg jumping exercises. Agility: walk and run in different directions. (20 min). Developing: weight training, based on the recommendations of the American Heart Association and the American College of Sports Medicine (45 to min). Cool-down: activities not reported (10 min). Stolzenberg et al., 2013 [34] Warm-up: cycle ergometry (15 min). Developing: one set of training using standard gym equipment. Finally, neuromuscular training including Romberg, Tandem and Single Leg Stance were performed on surfaces of varying degrees of instability and with varying degrees of difficulty: firm mat, soft mat, wobble board, air-pillows, with and without shoes, with eyes open or with eyes closed. Softballs, tennis balls, staves and elastic bands were used for coordination training. Warm-up and cool-down were not reported.

Neuromuscular Training
Tsauo et al., 2008. [35] Developing: sling suspension systems (TerapiMaster, Nordisk Terapi AS, Norway), where exercises in the supine, sitting and standing positions were performed sequentially. Warm-up and cool-down were not reported. * Time was not reported.
Regarding the duration of the interventions, three lasted six weeks [27,30,33], four lasted 8 weeks [26,28,32,35], two lasted 12 weeks [29,31] and one lasted 36 weeks [34]. Regarding the training frequency, all the studies reported a weekly distribution of two or three sessions. The minimum duration of a session was 15 min [34], while one study reported a duration of 80 min [26].
For the CG, in four studies the participants maintained their activities of daily living [28][29][30][31]. In two studies, the older people participated in physical fitness programs, which focused on exercises and activities to develop muscular endurance and strength, cardiorespiratory fitness, flexibility, agility, and postural balance [27,32]. Other investigations incorporated a routine of physical therapy including thermotherapy, interferential therapy and instructions for exercise at home [35], and the participants in the study by Stolzenberg et al. (2013) were trained on a vibrating platform [34]. Finally, Ahmad et al.
(2019) considered education on diabetic foot care as an intervention for the CG [26], while, in the study by Rezaeipour & Apanasenko, the participants had to remain seated for a period of time per week (60 min) [33].

Main Outcomes
The results of this systematic review show that neuromuscular training has beneficial effects on physical performance in older people. Of the 10 articles included in the review, nine of them reported significant changes in favor of the EG in at least one variable related to physical performance [26][27][28][29][30][31][32][33][34] compared to CG.
It was shown that neuromuscular training caused significant changes in postural balance in all the studies that included this variable as an outcome [26,27,[29][30][31][32][33][34]. One of the postural balance variables where a beneficial effect was evidenced was the COP, both with eyes open [26] and closed [26,34], which indicates a better postural balance. Specifically, the COP variables that decreased with the neuromuscular training were the COP sway [26], COP velocity [26,33], COP total mean velocity [33] and Romberg speed [31], which showed significant changes in the anteroposterior (AP) [26] and mediolateral (ML) directions [26,33]. The studies showed a decrease in the overall stability index [27,30], ML and AP stability indices [27] after the neuromuscular training. In addition, favorable balance changes were exhibited in the neuromuscular training groups in clinical postural balance tests such as FRT [26], TUG [26,33], OLS [26], Tinneti scale [31], Berg balance scale [29,31] and Four Square Step Test [29].
Finally, it was possible to determine the favorable effects of neuromuscular training on flexibility [32], cardiorespiratory fitness [32], strength and power of upper and lower limbs [32] and on functional autonomy [28].

Discussion
The objective of this systematic review was to analyse the scientific evidence regarding the effect of neuromuscular training on physical performance in older people. The main findings show that neuromuscular training has a positive and significant effect on some variables of physical performance, especially in postural balance. After reviewing 610 records, ten studies met the inclusion criteria; however, the quality of the research was only categorized as fair and good, with no excellent-quality studies. In terms of the risk of bias, five studies were categorized as high risk, while the remaining five had some concerns.
Among the main results of this systematic review is that seven of the articles included reported that a neuromuscular training program improves postural balance in older people, which is expressed in improvements in the stability indices, such as the COP variables [26,34], in functional tests, such as the TUG [26,33], OLS [26], FRT [26], and in the score of postural balance scales, such as the Berg scale [29,31] and Tinetti [31]. These results are in line with previous systematic reviews, where it has been reported that older women with osteoporosis who execute a neuromuscular training program improved static and dynamic postural balance, in addition to increasing the speed of motor responses [36]. Therefore, it has been suggested that this type of intervention would help improve the performance of activities of daily living and reduce the frequency of falls in older people [36].
When performing an exhaustive search of the literature, extensive benefits of neuromuscular training are reported, not only in functionality but also in the health and quality of life of people. However, neuromuscular training is still used more frequently in athletes and young people; for example, Vásquez-Orellana et al. (2022) demonstrated that a sixweek neuromuscular training program improves postural balance and proprioception in basketball players with functional ankle instability [37]. For their part, Guzmán-Muñoz et al. (2020) reported improvements in static and dynamic postural balance in obese children after only four weeks of neuromuscular training [38]. It has been suggested that neuromuscular training can enhance postural balance by stimulating anticipatory postural adjustments [39]. The repeated exposure to stability challenges on stable and unstable surfaces generates feedforward adjustments that would promote appropriate muscle activation [40]. Additionally, neuromuscular training could stimulate proprioception by inducing peripheral and central neural adaptations [17]. The central nervous system can use ascending information from the tendons (Golgi tendon organs), muscles (muscle spindles) and other mechanoreceptors (located in the ligaments, capsule and skin) to construct precise voluntary movements or to correct disturbances [41]. Consequently, the peripheral adaptations that may have occurred because of neuromuscular training likely resulted from the repetitive stimulation of the articular mechanoreceptors on both stable and unstable surfaces and in the eyes open and eyes closed conditions [38]. Therefore, neuromuscular training is mainly based on providing adequate sensory information to peripheral receptors so that the integration of muscular responses is more efficient, combining proprioceptive, strength and postural balance exercises [17,18]. This adjustment in motor responses would not only allow improvements in postural balance but also in other components of physical performance reported by the authors included in this review. In this way, it is suggested that neuromuscular training be used both in rehabilitation programs and in the prevention of injuries in older people [29]. The adaptations induced by neuromuscular training could be beneficial not only for athletes and young people, which suggests the need to develop studies that include this training methodology in the elderly population, given the anatomical, physiological and functional changes that occur with age.
On the other hand, two of the ten articles selected in this systematic review showed that older people who performed neuromuscular training improved performance in functional tests that assess muscle strength of upper and lower limbs compared to people from the CG [32,42]. In general, it has been established that older people have reduced muscle strength due to the anatomical changes that occur in the musculoskeletal system and the deterioration of sensory discrimination capacity [28]. Based on these antecedents, various authors have postulated that these deficiencies must be addressed specifically, where physical activity programs must not only be oriented towards isolated work on physical qualities but must include mixed activities, necessarily incorporating strength exercises, proprioception and postural balance-activities considered as the basis within a neuromuscular training program [43,44].
Finally, only one of the three studies selected for this review that included gait speed among its functional variables reported positive changes in favor of older people who performed neuromuscular training [30]. The divergence in the results found by the studies could be attributed to the heterogeneity of the tests used to assess walking speed, the differences in the distance traveled (60 m walk test and 10 m walk test), the different methodologies used to execute the test (normal walking speed or fast walking speed) or due to the different functional conditions and/or diseases that the older people in the studies had (sedentary older people and knee OA). Previous research has indicated that the discrepancy between the distance traveled and the pace of walking that is requested of the participants affects the results of the test [45]. Similarly, it remains unclear whether a longer walking distance yields a more accurate determination of gait speed than a shorter distance [45]. Regarding the speed that should be requested to perform the walk test at a normal pace, it seems to be more adequate to estimate the physical function and deterioration due to chronic disease [46]. Mobility is one of the most important aspects of physical function, especially as a prerequisite for performing activities of daily living. Given that walking is a complex motor phenomenon, resulting from the interaction of the nervous, musculoskeletal, vestibular and somatosensory systems, it is important to develop physical activity interventions that incorporate different motor skills with the aim of promoting the autonomy of older people.

Limitations
The main limitation of our systematic review is the low quality of the evidence found and the high risk of bias in the articles included. It is also worth mentioning the limited number of studies available, in which the participants were mainly women, and the heterogeneity found between the studies in terms of interventions (e.g., participants with different health statuses, duration of the session or sessions per week and the diversity of measurement instruments used). More evidence is needed to determine the real effects of neuromuscular training on the variables that make up physical fitness (cardiorespiratory fitness, muscle strength, flexibility, postural balance and agility) and to confirm the clinical relevance of these training-induced improvements.
In the same way, it is possible to recommend future studies with higher methodological quality, which include, among other aspects, double-blind evaluations and improvements in the randomization process of the sample, with the intention of clearly reporting the methodology used for the assignment of the participants to the different working groups. Finally, a strength of the present review was the strict inclusion/exclusion criteria (e.g., analyzing RCTs and quasi-experimental clinical trials).

Conclusions
Despite the limitation represented by the methodological quality of the available intervention studies, the evidence collected indicates that neuromuscular training has a positive and significant effect on some variables of physical fitness, especially in postural balance, so this type of training is seen as an effective resource to improve the functionality of the elderly and mitigate the deleterious effects caused by aging.

Data Availability Statement:
The data that support the findings of this study are available from the corresponding author upon reasonable request.