**E**ff**ects of Whole-Body Vibration Exercises on Parameters Related to the Sleep Quality in Metabolic Syndrome Individuals: A Clinical Trial Study**

**Claudia Figueiredo Azeredo 1,2, Patrícia de Castro de Paiva 1,2, Leandro Azeredo 3, Aline Reis da Silva 1,2, Arlete Francisca-Santos 2,4, Laisa Liane Paineiras-Domingos 2,4,5, Adriana Lírio Pereira da Silva 2, Camila Leite Bernardes-Oliveira 1,5, Juliana Pessanha-Freitas 2, Márcia Cristina Moura-Fernandes 2,6, Rubens Guimarães Mendonça 2, José Alexandre Bachur 7, Ygor Teixeira-Silva 2,5, Eloá Moreira-Marconi 2,6, Eliane de Oliveira Guedes-Aguiar 2,4,5, Bruno Bessa Monteiro de Oliveira 2,4, Mário Fritsch Neves 5, Luiz Felipe Ferreira-Souza 2, Vinicius Layter Xavier 8, Daniel Lago Borges 9, Ana Cristina Lacerda 10, Vanessa Amaral Mendonça 10, Anelise Sonza 11, Redha Taiar 12,\*, Alessandro Sartorio 13, Mario Bernardo-Filho <sup>2</sup> and Danúbia da Cunha de Sá-Caputo 2,4,5**


Received: 24 October 2019; Accepted: 22 November 2019; Published: 29 November 2019 -

**Abstract:** Metabolic syndrome (MetS) is an undesirable clinical condition with physiological, biochemical, clinical, and metabolic factors that contribute to increased cardiovascular risks (CR). A poor sleep quality might be found in obese and MetS individuals. Whole-body vibration (WBV) exercise has been used on the management of MetS individuals. This clinical trial investigated the effect of WBV exercise on parameters related to the sleep quality in MetS individuals. After randomization, nine individuals (seven women and two men) were exposed to a fixed frequency (FF) and ten individuals (eight women and two men) were exposed to a variable frequency (VF). Both groups performed the protocol twice a week, for 6 weeks. All of the evaluations were performed before the first and after the last sessions. Anthropometric and cardiovascular parameters were measured before and after the 6-week intervention. Pittsburgh Sleep Quality Index (PSQI), Epworth Sleepiness Scale (ESS), and Berlin Questionnaire were also used to evaluate the quality of the sleep. A significant (*p* ≤ 0.05) reduction of the waist circumference in the VFG and an increase of the heart rate were found in the FFG and VFG group. The score of the PSQI of the both groups decreased significantly (*p* = 0.01). The score of the ESS decreased (*p* = 0.04) only in the VF group. The scores of the Berlin Questionnaire were not altered in both groups. In conclusion, WBV intervention was capable in interfering with physiological mechanisms with effects on the WC and HR, leading to the improvement of the quality of sleep in MetS individuals. WBV exercise might be an important clinical intervention to the management of some factors associated with poor quality of sleep (FFG and VFG) and in the daytime sleepiness in MetS individuals with variable frequencies (5–16 Hz) (VFG).

**Keywords:** metabolic syndrome; sleep quality; whole-body vibration exercise; Pittsburgh Sleep Quality Index; Epworth Sleepiness Scale; Berlin Questionnaire

#### **1. Introduction**

Metabolic syndrome (MetS) is an undesirable clinical condition with physiological, biochemical, clinical, and metabolic factors, including alterations on the level of the lipids on the plasma, arterial hypertension, central adiposity, insulin resistance (IR), and hyperglycemia. These conditions strongly contribute to increased cardiovascular risks (CR) [1], and they are interconnected by pathophysiological basis in low-grade chronic inflammation, increase of the risk of type 2 diabetes mellitus (T2DM), and all-cause mortality [2]. MetS is also related to the increased deposit of central adiposity and ectopic fat infiltration (muscle and liver) associated with overeating and/or sedentary lifestyles. These conditions are related to various deleterious consequences in late life [3,4].

Lian et al. [5], in a systematic review and meta-analysis, reported that the overall sleep quality as well as sleep complaints have significant positive associations with MetS. Massar et al. [6] and Tsai et al. [7] pointed out that this condition of the sleep is linked with cardiovascular disease. Massar et al. [6] reported in individuals with poor habitual sleep efficiency during the week before stress induction (Trier Social Stress Test) responded with higher stress-related elevations of blood pressure and cortisol levels as compared to subjects with high sleep efficiency. This relationship between poor sleep efficiency and elevated blood pressure persisted during the post-stress recovery period. In addition, poor sleep health is also associated with MetS and mental illness [8,9]. Iftikhar et al. [10], in a meta-analysis reported that some investigations demonstrated the association between sleep quality and MetS. It was verified that the poor sleep quality characterized by sleep fragmentation was related to impaired glucose metabolism, independent of sleep duration [11], however, the studies of the meta-analysis analyzed had not reached a consensus. Mesas et al. [12] reported that the difficulty falling asleep is associated with MetS and, in particular, with high blood pressure, and this association would be independent of sleep duration and would be not due to lifestyles related to poor sleep.

Ying et al. [5] reported in a systematic review and meta-analysis that the overall sleep quality, as well as sleep complaints have significant positive associations with MetS. Moreover, it is estimated [13,14] that 50% to 60% of obese and MetS individuals can present obstructive sleep apnea (OSA).

Some tools have been used to verify parameters (such as sleep duration, sleep inertia, sleep latency, snoring, disorientation or confusion during sleep, and daytime sleepiness) related to the quality of the sleep, such as the Pittsburgh Sleep Quality Index (PSQI) [15], Epworth Sleepiness Scale (ESS) [16] and the Berlin Questionnaire [17]. Moreover, the neck circumference (NC) [16] and waist circumference (WC) [18,19] have also been used.

There is moderate evidence supporting the use of physical exercise (PE) programs to counter MetS, although the optimal dose and type of PE is not well established. It is the main challenge for health care professionals to persuade individuals to have adherence to perform PE to the prevention and management of MetS [20]. In this case, it is relevant to consider the whole-body vibration (WBV) exercise, a modality of PE, an option. WBV exercise has been used as a clinical intervention in individuals with different clinical disorders, including MetS [21–26] and it can be considered a feasible, safe, and low-cost technique [27].

WBV exercise is generated in an individual who is on the base of a vibrating platform. It produces a mechanical vibration (MV) that is transmitted to the body inducing muscle contractions, with physiological responses like those produced by other types of PE, such as aerobic conditioning and strength training [28–30]. Biomechanical parameters, such as the frequency (*f*) and the peak-to-peak displacement (PPD) of the MV must be considered in the WBV exercise protocols [26,31,32].

As it is suggested that the sleep quality plays an important role in development of MetS [5] and putting together all of the previous considerations, to our knowledge, this is a first work aiming to study the effect of WBV exercise on the sleep quality of MetS individuals using the PSQI, ESS, and Berlin Questionnaire. It is hypothesized that the WBV exercise would be able in improving the sleep quality of MetS individuals.

#### **2. Materials and Methods**

#### *2.1. Individuals*

In this cross-sectional and randomized study, 31 subjects were recruited and 19 performed the protocol (58.79 ± 12.55 years old, 1.62 ± 0.09 m height, 86.27 ± 15.03 kg body mass). The recruitment of the participants occurred from January 2018 to January 2019, in the *Hospital Universitário Pedro Ernesto* (HUPE), in the *Universidade do Estado do Rio de Janeiro* (UERJ). The WBV protocol was performed in the *Laboratório de Vibrações Mecânicas e Práticas Integrativas* (LAVIMPI).

This project was approved by the Research Ethics Committee of HUPE-UERJ with the number CAAE 54981315.6.0000.5259, the registry in the Brazilian Registry of Clinical Trials (ReBEC) with the number RBR 2bghmh and UTN: U1111-1181-1177. The participants of both groups signed a consent form.

Consolidated Standards of Reporting Trials (CONSORT) was used to report all of the different steps of the interventions utilized in this work [33].

In the randomization, a blinded envelope was used for the cards with the name of the groups: fixed frequency group (FFG) (control group) or variable frequency group (VFG) (WBVE group).

The inclusion criteria were individuals of both sexes, over 18 years of age, with MetS according to the International Diabetes Federation.

The exclusion criteria were: (i) individuals with high blood pressure (BP) levels (systolic blood pressure (SBP) ≥ 180 mmHg and diastolic blood pressure (DBP) ≥ 110 mmHg); (ii) cardiovascular disease (CVD) clinically evident in the last 6 months, manifested by a myocardial infarction or a stroke; (iii) a neurological, muscular, or rheumatologic disease that difficulte the position of the individual on the vibrating platform; (iv) disabling clinical disease according to the evaluation; (v) speech therapy or respiratory physiotherapy in the last 3 months; (vi) body mass index (BMI) > 40 kg/m2; (vii) orthodontic therapy with intraoral device; (viii) individuals who refuse to sign the consent form.

The participants declared that they were sedentary. They were instructed to continue their daily activities, dietary habits, and medications during the period of the investigation. The drugs used by the participants of both groups were diuretics, beta blockers, calcium channel blockers, angiotensin converting enzyme inhibitors, and angiotensin receptor antagonists.

#### *2.2. Interventions*

#### 2.2.1. Fixed Frequency Group (Control Group)

After the randomization, nine individuals (seven women and two men) allocated in the FFG performed a protocol twice a week, for 6 weeks. In this protocol, the individuals were positioned in a squat position, barefoot and with 130◦ knee flexion (Figure 1A). The biomechanical parameters were 2.5, 5 and 7.5 mm (Figure 1B–D) of PPD and 5 Hz for 10 s of vibration and 110 s of non-vibration in each bout. From 1 to 4 weeks, were performed 3 bouts in each session, totaling 18 min of total time. From 5 to 8 weeks, were performed 4 bouts in each session, totaling 24 min of total time. From 9 to 12 weeks, were performed 5 bouts in each session, totaling 30 min of total time. The participants performed dynamic and static squats in the sessions.

**Figure 1.** Biomechanical parameters during the intervention (fixed frequency (FF) and variable frequency (VF) groups) using the side alternating vibratory platform; (**A**) individual in a stand position, barefoot and with 130◦ knee flexion; (**B**) individual in 2.5 mm of peak-to-peak displacement (PPD) on the base of the vibrating platform with medial malleoli together; (**C**) individual in 5 mm of PPD on the base of the vibrating platform 21 cm apart between the medial malleoli; (**D**) individual in 7.5 mm of PPD on the base of the vibrating platform 38 cm apart between the medial malleoli.

#### 2.2.2. Variable Frequency Group (WBVE Group)

After the randomization, ten individuals (eight women and two men) allocated in the VFG performed the protocol twice a week, for 6 weeks. In this protocol, the individuals were positioned in a squat position, barefoot and with 130◦ knee flexion (Figure 1) The biomechanical parameters of the MV were 2.5, 5 and 7.5 mm (Figure 1B–D) of the PPD; the frequency was 5 Hz in the first session and it increased by one Hz in each session, and it was 16 Hz in the last session. During the intervention, were performed 60 s of MV and 60 s of non-vibration in each bout. From 1 to 4 weeks were performed 3 bouts in each session, for a total time of 18 min. From 5 to 8 weeks, were performed 4 bouts in each session, for a total time of 24 min. From 9 to 12 weeks were performed 5 bouts in each session, for a total time of 30 min. Dynamic and static squats were performed in interspersed sessions.

#### *2.3. Anthropometric Measurements and Physiological Parameters*

All of the measurements were performed in the same location, at room temperature. Height and body mass were measured on a digital balance (MIC 200 PPA, Micheletti, São Paulo, Brazil). The BMI was calculated by dividing body mass (in kg) by square of height (in m) [34]. WC was obtained with a flexible measuring tape connecting the midpoints between the last costal arch and iliac crest, at the end of the soft exhalation and in the orthostatic position [34]. NC was obtained using a flexible metric tape just below the prominence of the larynx [35].

An automated device (OMRON, model HEM-7113, Dalian, China) was utilized to record the SBP and DBP (mm Hg), and the HR (beats/min) was measured on the left arm of seated patient after a 10-min rest. Three measurements were performed with 1 min of rest after each measurement. The mean of these 3 records of SBP and DBP and HR was used in the analyses of the WBV exercise group and the control group [36]. These evaluations were performed before and after the 6-week intervention in both groups.

The data of these parameters were expressed in mean and standard derivation and the Wilcoxon rank test was performed.

#### *2.4. Questionnaires*

The PSQI [15] was used to assess sleep quality and disturbances over a 1-month period. This questionnaire is composed of 19 self-rated questions and 5 questions that should be answered by bedmates or roommates. The 19 questions are separated into 7 categories and there is a score from 0 to 3. The components of this questionnaire are subjective sleep quality, sleep latency, sleep duration, habitual sleep efficiency, sleep disturbances, use of medication, and daytime dysfunction. The maximum PSQI score is 21 points. Higher scores indicate poor quality of sleep [37].

The ESS [16] is composed of 8 self-reported questions and it is used to assess the self-reported level of daytime sleepiness [38]. These items have a four-point scale (0 indicating "would never nod off" and 3 indicating a "strong chance of nodding off"). The questionnaire questions are related to daily activities. The questionnaire score ranges between 0 and 24. Higher total scores are related to more sleepiness [39].

The Berlin Questionnaire [17] has been proposed as a tool in screening OSA and validated in primary care. The subjects were classified into high risk (if there were 2 or more categories where the score was positive), and low risk (if there was only 1 or no categories where the score was positive). The percentage os individuals with high risk to OSA was calculated in both groups [40,41].

The PSQI, ESS, and Berlin Questionnaire were only measured before and after the 6-week intervention in both groups.

#### *2.5. Statistical Analyses*

For the sample size calculation, we used a standard deviation of 3.1, a margin of error of 2, the significance level of 5%, and a sample size of 9 individuals in each group, considering the PSQI [42].

The Wilcoxon signed-rank test with continuity correction was used in the analyses of the DBP, SBP, HR, WC, NC, the PSQI, and ESS. Descriptive statistics, median, and interquartile range (IQR) are also reported. Wilcoxon signed-rank test is a nonparametric test that was used to determine if paired samples, before and after intervention, have the same distribution. Fisher's exact test was

applied to the qualitative variable, Berlin, to asses if the proportion of people in each class (high risk and low risk) have been affected by the experiment. In the analyses of the PSQI and ESS, the values are expressed in scores. The statistical analyses of the Berlin Questionnaire considered only the percentage of individuals with a high risk to OSA.

All statistical analysis was performed using R software, version 3.5.0 [43] and the R Librarie Table 1 [44]. Results are considered statistically significant if the *p*-value is under 0.05 (*p* ≤ 0.05).

#### **3. Results**

The flow diagram with the enrolment of the study is shown in Figure 2. Thirty-one individuals were recruited, two individuals were excluded because they did not have risk of sleep apnea, three declined to participate, and seven individuals declined due to other reasons (economical problem related to the transportation).

**Figure 2.** Flow diagram of the intervention.

Table 1 shows some anthropometric parameters of the individuals that were exposed to WBV exercise (FV group) and to only 5 Hz (FF group). An analysis is shown of both groups before and just after the treatments. It was verified that the BMI, NC, SBP, and DBP (*p* > 0.05) were not significantly altered in both groups. However, a significant increase in the HR (*p* < 0.05) was found in both groups exposed to mechanical vibration, only 5 Hz (FFG) and variable frequency 5–16Hz (VFG). Furthermore, a reduction was found in the group that was submitted to the variable frequency 5–16 Hz (VFG) in the WC.


**Table 1.** Anthropometrical parameters of the individuals exposed to variable frequency group (intervention 5–16 Hz) and to only 5 Hz (fixed frequency group).

BMI—body mass index, WC—waist circumference, NC—neck circumference, SBP—systolic blood pressure, DBP—diastolic blood pressure, HR—heart rate, FF—fixed frequency group, VF—variable frequency group.

Figure 3 shows the values of the scores of the PSQI of the individuals of the group exposed only to mechanical vibration of 5 Hz (FFG-control). A significant decrease was found (p = 0.01) of the score (after and before) of the individuals of the FF group (exposure to 5 Hz).

**Figure 3.** Scores of the Pittsburgh Sleep Quality Index (PSQI) of the individuals of the group exposed only to a mechanical vibration of 5 Hz (FFG) (before and after).

Figure 4 shows the values of the scores of the PSQI of the individuals of the groups exposed to the treatment with WBV exercises (VFG). It is observed that an important and significant (*p* = 0.008) decrease of score in the group after the exposure to various frequencies (intervention) was seen. This finding indicates an improvement of quality of the sleep.

**Figure 4.** Scores of the PSQI of the individuals exposed to the whole-body vibration (WBV) intervention with variable frequency (VFG).

Figure 5 shows the values of the scores of the ESS of the individuals of the group exposed only to mechanical vibration of 5 Hz (FFG). It is observed that there was no significant decrease (*p* = 1.0) of the score (after and before) of the individuals. This finding indicates no reduction of daytime sleepiness.

**Figure 5.** Scores of the Epworth Sleepiness Scale (ESS) of the individuals of the SG individuals of the FFG (before and after).

Figure 6 shows the values (before and after the interventions) of the scores of the ESS scale of the individuals of the groups exposed to the treatment with WBV exercises (VFG). It is observed that there

was a significant (*p* = 0.04) decrease of the score in the group after the exposure to various frequencies (intervention). This finding indicates a reduction of daytime sleepiness.

**Figure 6.** Scores of the ESS of the individuals of the group exposed to the intervention with WBV exercises (VFG).

Considering the Berlin Questionnaire, no alteration in ter percentage of individuals with risk to OSA were significantly found in both groups, the FF *p* = 0.29 and FVG *p* = 1.00.

#### **4. Discussion**

The underlying etiology of MetS is multifactorial, however, they are not well known, but sedentary lifestyles and unhealthy dietary habits favor the appearance of MetS [45]. Considering the high prevalence and strong and undesirable complications, early identifying and controlling the modified risk factors are key prevention methods to counter the development of MetS and its progression to CVD.

It is relevant to point out that, to our knowledge, this is the first work that was performed to evaluate the effect of WBV exercise in sleep quality of MetS individuals. As it was hypothesized that the WBV exercise would be able to improve the sleep quality of MetS individuals, the quality of sleep was improved (PSQI) and a reduction of daytime sleepiness (ESS) in the MetS was found due to a protocol with variable frequencies (5–16 Hz) of WBV. A protocol with fixed frequency (5 Hz) also improved the quality of sleep (PSQI).

It was shown (Table 1) that the 6-week intervention with WBV exercise with variable frequencies (from 5 up to 16 Hz) (VF group) did not alter significantly the BMI, NC, SBP, and DBP. The same finding was verified in the individuals with fixed frequency (5 Hz). These findings agree with other studies. Feairheller et al. [46], in a study of six months, have shown that aerobic exercise training is enough to elicit improvements in vascular structure and function in African Americans, even without alterations on BP measurements (SBP and DBP) in African Americans. Moreover, Sá-Caputo et al. [31] have reported that, in individuals with MetS exposed to acute WBV exercise, the SBP and DBP were not altered. Figueroa et al. [21] have reported that the BMI of overweight/obese women was not modified after 6 weeks of WBV exercises.

Considering the HR (Table 1), an increase was verified in FFG (only 5 Hz) and VFG (variable 5–16 Hz), and this is in agreement with Sunita et al. [47] that have also observed an increase of the HR in response to exercise. Moreover, Kang et al. [48] have described an association between resting HR and cardiorespiratory fitness with an elevated resting HR.

The findings presented in Table 1 indicated no alterations on SBP and DBP due to WBVE (a possible stressor), however, Massar et al. [6] reported that individuals with poor habitual sleep efficiency during the week before stress induction (Trier Social Stress Test) responded with higher stress-related elevations of blood pressure and cortisol levels as compared to subjects with high sleep efficiency.

In the current study, no alterations on the NC were found. However, a decrease on the WC was found (Table 1). Sîrbu et al. [49] have compared some anthropometric parameters in trained and sedentary healthy young students. It was found that in moderately aerobic trained students, the BMI and BP were not significantly different between the two groups. However, a significantly lower NC was found in the trained students. Considering the WC, in agreement with our results, King et al. [50] have verified that a 12-week supervised aerobic exercise intervention has reduced significantly the WC of overweight/obese men and women. But, Sîrbu et al. [49], have not found alteration in the WC due to exercise.

WBV exercise is an intervention with several improvements in populations with various diseases [23–25,31]. In this current study, it was verified that WBV exercise has improved the quality of the sleep in MetS when we used the PSQI (Figures 3 and 4) and ESS (Figure 6). This finding is partially in agreement with Souza et al. [51] who have evaluated, in a population of 16 individuals with OSA, the effectiveness of inspiratory muscle training (IMT) on sleep and functional capacity to exercise. It was a significant improvement in sleep quality was seen with PSQI values, but no significant changes were seen in daytime sleepiness (ESS) after the intervention. Furthermore, Reid et al. [52] have verified that moderate aerobic PE improved the sleep quality of sedentary adults considering the PSQI and the ESS. Brandão et al. [53] have reported that home exercise improves the quality of sleep and daytime sleepiness of elderlies considering, respectively, the PSQI and the ESS.

The findings of the current work have verified that the sleep quality was not altered when the Berlin Questionnaire was used. This result agrees with Brandão et al. [53] who have reported that home exercise does not alter the risk to OSA when the same questionnaire was used.

Kline et al. [54], evaluated the utility of PE for improving daytime functioning in adults with OSA. Sleepiness and functional impairment due to sleepiness also were improved following exercise versus control, though these changes were not statistically significant. It is suggested that PE may be helpful for improving aspects of daytime functioning of adults with OSA. Moreover, Yilmaz Gokmen et al. [55] have investigated the effects of Tai Chi and Qigong training on severity of OSA for 12-weeks. In the intervention group, there was a statistically significant decrease in the ESS. However, Itoh et al. [56], in a cross-sectional study among non-obese male workers in Japan, found no significant association between physical activity and the risk of sleep-disordered breathing.

Considering the MetS, not all forms of exercise are equally effective and safe; although aerobic exercise [57] or resistance training have been associated with decreased cardiovascular disease risk factors, obesity, or MetS severity [58,59]. Due to the pain or even the low physical fitness, most individuals are unable or unwilling to perform these exercises [60]. Given the limitations for some types of exercises that many individuals report, different forms of exercise are being suggested for MetS individuals [61]. WBV exercise has improved several parameters in MetS individuals [26,31,32] and in the current study a decrease of the WC was found (Table 1).

This study has some limitations, no control of daily activity, daily working, lifestyle habits, smoking, PE, and daily energy intake. The follow-up data were not available after the intervention. The external validity of this intervention considering its generalizability to other settings (like the everyday-living condition) was not explored and only a small sample was used. The big ratio of female to male would be also considered as a limitation of the study. Moreover, a sham group and a group of individuals without MetS were not used. Furthermore, the analysis of the questionnaires was not done in the weeks in which there were changes of the frequency and duration of the intervention in the VFG. Some points of the questionnaires are influenced by factors that are not taken into account in the current

study, as categories of individuals (good-sleepers and bad-sleepers), sleep duration, sleep inertia, and sleep latency. In consequence, further investigations are required. However, putting together all the considerations, the strength was to verify that a WBV exercise might be suggested as an option to the management of MetS individuals with some important outcomes, and it would be expected that a WBV exercise might lead to responses that can reflect in improvements of the sleep quality.

#### **5. Conclusions**

In conclusion, WBV intervention was capable of interfering with physiological mechanisms with effects on the WC and HR, leading to the improvement of the quality of sleep in MetS individuals. Although the calculated sample size determined a study with a small number of individuals, WBV exercise might be an important clinical intervention to the management of some factors associated with poor quality of sleep (FFG and VFG) and in the daytime sleepiness in MetS individuals with variable frequencies (5–16Hz) (VFG). However, further investigations are necessary to try to understand the mechanisms that underlines this positive effect of the WBV exercise in the studied population, as well as with individuals with sleep disturbances without MetS.

**Author Contributions:** Conceptualization, R.T., A.S. (Alessandro Sartorio), M.B.-F., and D.d.C.d.C.D.S.-C.; data curation, C.F.A., J.A.B., V.L.X., and D.L.B.; formal analysis, J.A.B., V.L.X., D.L.B., A.C.L., V.A.M., A.S. (Anelise Sonza), and R.T.; funding acquisition, M.B.-F.; Investigation, C.F.A., P.d.C.d.P., L.A., A.R.d.S., A.F.-S., L.L.P.-D., A.L.P.d.S., C.L.B.-O., J.P.-F., M.C.M.-F., R.G.M., Y.T.-S., E.M.-M., E.d.O.G.-A., B.B.M.d.O., M.F.N., and L.F.F.-S.; methodology, C.F.A., P.d.C.d.P., L.A., A.R.D.S., A.F.-S., L.L.P.-D., A.L.P.d.S., C.L.B.-O., J.P.-F., M.C.M.-F., R.G.M., J.A.B., Y.T.-S., E.M.-M., E.d.O.G.-A., B.B.M.d.O., M.F.N., L.F.F.-S., and A.S.(Alessandro Sartorio); project administration, M.B.-F. and D.d.C.d.C.D.S.-C.; resources, C.F.A., P.d.C.d.P., L.A., A.R.d.S., R.G.M., and B.B.M.d.O.; software, V.L.X.; supervision, M.B.-F. and D.d.C.d.C.D.S.-C.; validation, V.L.X., M.B.-F., and D.d.C.d.C.D.S.-C.; visualization, A.S.(Anelise Sonza) and R.T.; writing—original draft, C.F.A.; Writing—review and editing, A.C.L., V.A.M., A.S. (Anelise Sonza), A.S. (Alessandro Sartorio), M.B.-F., and D.d.C.d.C.D.S.-C.

**Funding:** This study was supported in part by the *Coordenação de Aperfeiçoamento de Pessoal de Nível Superior* - Brazil (CAPES) - Finance Code 001, the *Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro* (FAPERJ).

**Conflicts of Interest:** There is no conflict of interest.

#### **References**


© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).

*Article*

**Cintia Renata de Sousa-Gonçalves 1,2, Laisa Liane Paineiras-Domingos 1,2,3, Ygor Teixeira-Silva 1,2, Thais Amadeu 1, Adriana Pereira da Silva Lírio2, Arlete Francisca-Santos 2, Luiz Felipe Ferreira De Souza 2, Mario José dos Santos Pereira 2, Maria Eduarda Souza Melo-Oliveira 2,4, Alexandre Gonçalves de Meirelles 2,4, Glória Maria Guimarães-Lourenço 2,4, Aline Reis-Silva 2,4, Eloá Moreira-Marconi 2,5, Marcia Cristina Moura-Fernandes 2,5, Vinicius Layter Xavier 6, Alessandra da Rocha Pinheiro Mulder 7, Ana Cristina Rodrigues Lacerda 8, Vanessa Amaral Mendonça 8, José Alexandre Bachur 9, Redha Taiar 10,\*, Alessandro Sartorio 11, Danúbia da Cunha de Sá-Caputo 1,2,3 and Mario Bernardo-Filho <sup>2</sup>**


Received: 16 October 2019; Accepted: 15 November 2019; Published: 20 November 2019 -

**Abstract:** Metabolic syndrome (MetS) is related to overweight and obesity, and contributes to clinical limitations. Exercise is used for the management of MetS individuals, who are often not motivated to perform this practice. Whole body vibration exercise (WBVE) produces several biological effects, besides being safe, effective, and feasible forMetS individuals. This pseudo-randomized and cross-over controlled trial study aimed to analyze the effects of WBVE on MetS individuals' neuromuscular activation using the surface electromyography (sEMG) pattern (root mean square (RMS)) of the vastus lateralis (VL) muscle and on the range of motion (ROM) of the knees. Participants (n = 39) were allocated to two groups: the treatment group (TG), which was exposed to WBVE, and the control group (CG). WBVE interventions were performed twice a week, for a period of 5 weeks. ROM and sEMG were analyzed at baseline, after the first session, and before and after the last session. sEMG (%RMS) significantly increased in the acute effect of the last session of WBVE (108.00 ± 5.07, p < 0.008, right leg; 106.20 ± 3.53, p < 0.02, left leg) compared to the CG. ROM did not significantly change in TG or CG. In conclusion, 5 weeks of WBVE exerted neuromuscular effects capable of increasing VL muscle RMS in individuals with MetS, this effect being potentially useful in the physical rehabilitation of these individuals.

**Keywords:** metabolic syndrome; whole body vibration exercise; range of motion of the knees; surface electromyographic pattern; neuromuscular activation; biomechanics

#### **1. Introduction**

In the modern world, unhealthy lifestyles, including physical inactivity and bad dietary habits, contribute to the development and spread of diseases associated with metabolic commitment, such as metabolic syndrome (MetS). MetS is defined as a clustering of metabolic abnormalities, such as central obesity (increased waist circumference), dyslipidemia, hyperglycemia, and hypertension, according to the guidelines of the International Diabetes Federation (IDF) [1,2].

Yang et al. pointed out that overweight and obesity are emerging major health issues, which are closely related MetS [3]. Body mass excess can promote adipose tissue stored in the abdominal cavity and intramuscular adipose tissue (IMAT) [4,5]. It is known that these conditions directly affect the biomechanics of movements [6–8], leading to decreased mobility, strength, and ability to perform common activities of daily living [6,9,10]. In obese individuals, lower extremity overuse injury is caused by multiple mechanisms, including increased load bearing with ambulation, altered gait biomechanics due to abnormal body mass distribution, a systemic pro inflammatory state [7,11–13]. The affected joint kinetics may increase the risk of musculoskeletal injury, with the development of osteoarthritis, especially in the knees [7,14], and the impairment of the range of motion (ROM) [7,15]. Reduced ROM can imply the limitation of the knee flexion [15], which is required to perform activities of daily living [16]. ROM is a parameter of physical evaluation, since it can allow the identification of joint and muscle limitations. Moreover, it is used for the evaluation of individuals during the rehabilitation process [17].

In obese individuals, the lower limb muscles (flexors and extensors) are frequently committed [9,10]. In consequence, decrease of muscle strength and power, and premature fatigue [6] are observed, leading to impaired motor performance [18]. As these individuals are not motivated to practice regular exercise, methods to increase adherence including exercises that minimize the impact on the joints are necessary [19]. Among the different kinds of exercises, whole body vibration exercise (WBVE) may be an option for the management of obese individuals [20,21].

WBVE involves exposing individuals to mechanical vibrations that are produced in a vibrating platform (VP). These vibrations are transmitted to the body of the individual that is in contact with the base of the VP. Some parameters must be adjusted (frequency, peak-to-peak displacement, and peak acceleration) considering the clinical condition of the individual [22]. Similarly, if the person is sitting on an auxiliary conventional chair [23] or wheelchair [24] with the feet on the base of VP, the individual will also experience WBVE.

Authors evaluated the effects of WBVE on MetS individuals, and important responses were observed, such as improvement of quality of life and flexibility [25,26]. Moreover, WBVE is safe and effective to treat muscle complications in populations with different disorders [27–31] as well as healthy individuals [32,33].

Surface electromyography (sEMG) is an adequate tool to evaluate neuromuscular effects of WBVE [27,34–36]. An increased sEMG activity after WBVE indicates that more motor units are recruited [34].

It is well described that WBVE can improve joint mobility [29,37,38]. Moreover, Wang et al. found that WBVE in combination with quadriceps resistance exercise compared with quadriceps resistance exercise alone showed significantly greater improvement in knee flexion and extension in individuals with knee osteoarthritis [39].

The aim of this study was to analyze the effects of WBVE on neuromuscular activation through the electromyographic pattern of the vastus lateralis muscle and on range of motion of the knees in MetS individuals. The study hypothesis was that WBVE would increase neuromuscular activation and range of motion of the knees of MetS individuals.

#### **2. Materials and Methods**

This was a quasi-randomized cross-over controlled trial, where 39 individuals with MetS were selected to evaluate the effect of WBVE on neuromuscular activation and range of motion of the knees. Individuals were allocated, as they arrived, to the control (CG) or treatment group (TG). The study protocol was approved by the Research Ethics Committee of the Hospital Universitário Pedro Ernesto (HUPE), Universidade do Estado do Rio de Janeiro (UERJ), with the number CAAE 54981315.6.0000.5259, and was registered in the Registro Brasileiro de Ensaios clínicos (ReBEC) (RBR 2bghmh).

Recruitment took place from April 2014 to January 2016 following screening of MetS individuals by the medical staff at HUPE-UERJ, Brazil. The WBVE protocol was performed in the Laboratório de Vibrações Mecânicas e Práticas Integrativas (LAVIMPI), UERJ. Participants signed a consent form before any procedures, and the principles embodied in the Declaration of Helsinki were followed.

#### *2.1. Sample Size*

The sample size was determined based on a study by Sá-Caputo et al. [26], involving individuals with MetS exposed to WBVE, using an online calculator of the Laboratório de Epidemiologia e Estatística (LEE), Faculdade de Medicina, USP, São Paulo, Brazil [40]. For a statistical power of 95%, a sample size of 13 individuals was calculated [26,40]

#### *2.2. Inclusion and Exclusion Criteria*

For this study, the inclusion criteria were age over 40 years (male and female gender) and a diagnosis of MetS. All participants were selected by a clinical physician, who diagnosed MetS according to the International Diabetes Federation criteria [1].

The exclusion criteria comprised very high blood pressure (≥180/110 mmHg), cardiovascular disease (coronary artery disease or stroke), neurological, musculoskeletal, or rheumatologic disease that do not permit to be on the VP, refusal to sign the consent form for participation in the study, and fear of being on the VP due to its movements.

#### *2.3. Interventions*

Eligible participants (n = 39) were allocated to one of two groups: TG and CG. In the TG, the individuals performing the protocol with the VP turned on, while in the CG, the VP was turned off. After a 2-month washout (i.e., the period of time between the two interventions), the participants were crossed-over to the other group [41]. All procedures were performed by health professionals previously trained by experienced trainers to perform this protocol. Intra-rater reliability was not

performed. The VP (Novaplate Fitness Evolution, DAF Produtos Hospitalares Ltda., São Paulo, Brazil) was a side alternating platform, in which the right site is displaced down while the left side is displaced up, and vice versa [26,42].

In the first session of the TG, all the individuals were seated on a chair placed in front of the platform with a 130◦ knee flexion. Their feet, shoeless, were placed on the base of the platform, alternately in three positions (peak to peak displacements of 2.5, 5.0, and 7.5 mm) and with a frequency of 5 Hz. The working time in each position was 1 minute followed by 1 minute of rest. This sequence was performed three times. This procedure is shown in Figure 1.

**Figure 1.** Individual performing whole-body vibration exercise seated on a chair placed in front of the vibrating platform.

From the second to the last session (10th session), the individuals were subjected to exactly the same protocol of the first session; however, they were standing on the base of the VP in a squat position (130◦ knee flexion), and the frequency was progressively increased by 1 unit per session up to 14 Hz in the last session. The WBVE session was performed twice per week during 5 weeks. This procedure is shown in Figure 2.

**Figure 2.** Individual performing WBVE in a standing position on the vibrating platform.

#### *2.4. Outcome Measures*

#### 2.4.1. Anthropometric Evaluation

Anthropometric data (body mass, height) of the participants were assessed by a single operator using a balance with a stadiometer (Micheletti MIC 200PPA, São Paulo, Brazil). The waist circumference (WC) was measured with a tape in the horizontal plane, midway between the inferior margin of the ribs and the superior border of the iliac crest, in agreement with the IDF recommendations [1]. The body mass index (BMI) was calculated dividing body mass in kilograms by squared height in meters [43].

#### 2.4.2. Evaluation of Knee Range of the Motion

A standard digital goniometer (EMG 830RF, EMG*System*®, São Paulo, Brazil) was used to measure the active ROM [44–46] of the knees during flexion from extension. The goniometer was properly fixed on the skin with tape on the lateral side of the knee joint, alternately right and left, to measure the flexion angle. Knee angles related to ROM were recorded on a computer. These procedures are shown in Figure 3.

**Figure 3.** Position of the goniometer on the lower limb for measurement of knee range of motion (ROM).

ROM was determined before and after the first session (acute effect of the first session). The same procedure was performed in the last session (acute effect of the last session). In addition, comparisons were made before the first session and before the last session (cumulative effect) [47]. The percentage of the alteration of ROM (%AROM) in each condition was calculated dividing the ROM after the session by the ROM before the intervention (acute effect of the first and of the last session) multiplied by 100. The %ROM to the cumulative effect in each condition was calculated by dividing the value of ROM before the last session by the ROM before the first session multiplied by 100.

#### *2.5. Surface Electromyography (sEMG) Instrumentation and Measurement*

The neuromuscular activity of the vastus lateralis (VL) muscle was evaluated following the recommendations of the Surface ElectroMyoGraphy for the Non-Invasive Assessment of Muscles (SENIAM) regarding skin preparation and fixation of the electrodes in the specified positions related to the VL muscle [48], and the reference electrode was positioned on the spinous process of C7. The sEMG signal was collected in microvolts (μV) in a computer and was analyzed using the root mean square (RMS) (EMG832WF, EMG*System*®, São Paulo, Brazil). In the sEMG assessment, the individuals were asked to sit on a chair with the back straight, feet approximately shoulder-width apart and placed on the floor, and the arms crossed over the chest. Then, they were instructed to perform five repetitions of sitting and standing [49].

The RMS amplitude signal was recorded before and after the first session (acute effect of the first session), and before and after the last session (acute effect of the last session). The %RMS in each condition was calculated dividing the RMS after the session by the RMS before the session (acute effect of the first and of the last session) multiplied by 100. The %RMS to the cumulative effect was calculated in each condition by dividing the value of the RMS before the last session by the RMS before the first session multiplied by 100.

#### *2.6. Statistical Analysis*

Statistical analyses were performed using GraphPad Prism 6. The normality of the data was evaluated with the Shapiro-Wilk test. For the comparison of paired nonparametric values, the Wilcoxon Signed-Rank test was used. For the comparison of the two groups (TG and CG), the Mann Whitney test was used. The comparison of the cumulative effect of ROM between the groups was performed using the difference (Δ) between the value before the first session and that after the last session. The difference was considered significant when p ≤ 0.05. The descriptive statistics used were mean and standard error, since the focus of the work was the effect of the intervention.

#### **3. Results**

The anthropometric data of the participants are reported in Table 1. There were no significant differences between the two groups (p > 0.05). According to IDF [2], participants with increase in WC values have more probability to develop MetS.


**Table 1.** Anthropometrics data of the individuals of the study.

CG: control Group; TG: treatment group; SE: standard error; BMI: body mass index; WC: waist circumference.

The acute effects of WBVE on the ROM of the right and left knees in the first session are shown in Table 2. No significant changes in ROM were observed in either of the groups (CG and TG) or in the comparison between them. Although no significant differences (p > 0.05) were detected, the %AROM of the right knee of the participants in the CG decreased slightly (85.65%), while that of the left knee increased slightly (107.21%). The %AROM of the right and left knees of the participants in the TG decreased slightly (98.09% and 98.10%, respectively).

**Table 2.** Acute effects on range of the motion of right and left knees in the first session.


CG: control group; TG: treatment group; SE: standard error.

Table 3 shows the acute effects of WBVE on the ROM of the right and left knees in the last session. No significant changes were observed in either of groups (CG and TG) or in the comparison between CG and TG. Although no significant differences (p > 0.05) were detected, the %AROM of the right knee and of the left knee of the participants in the CG increased slightly (102.17% and 103.96%, respectively). The %AROM of the right knee of the participants of the TG decreased slightly (98.67%), and that of left knee increased (102.04%).


**Table 3.** Acute effects on range of the motion of right and left knees in the last session.

CG: control group; TG: treatment group; SE: standard error.

The cumulative effects of WBVE on the ROM of both knees (i.e., value of ROM before the first session vs. the value before the last session) is reported in Table 4. Although no significant differences were detected in the TG or CG, an improvement of 7.5 and 13.51 degrees in ROM was observed in the TG on the left and right knee, respectively. Moreover, the %AROM of the right knee of the participants in the CG decreased slightly (98.53%), and that of the left knee increased (105.79%). The %AROM of the right and left knees of the participants in the TG increased importantly (114.29% and 107.44%, respectively).

**Table 4.** Cumulative effects on range of the motion of right and left knees before the first session vs. before the last session.


CG: control group; TG: treatment group; SE: standard error.

Using sEMG, Table 5 shows the response of the vastus lateralis muscle of both legs to the acute effect of WBVE in the first session, in %RMS. No significant effects were found (left or right legs) in TG or CG.

**Table 5.** Acute effects on electromyography (%RMS) of vastus lateralis muscles (right and left) in the first session.


CG: control group; TG: treatment group; SE: standard error; %RMS: percentage of the root mean square; VL: vastus lateralis muscle.

The acute effects of WBVE on sEMG of the vastus lateralis muscles in the last session are shown in Table 6. Significant increases (p < 0.05) were observed on the %RMS of vastus lateralis muscles on both legs of the TG relative to the CG.


**Table 6.** Acute effects on electromyography (%RMS) of vastus lateralis muscles (right and left) in the last session.

CG: control group; TG: treatment group; SE: standard error; %RMS: percentage of the root mean square; VL: vastus lateralis muscle; p ≤ 0.05 \*.

The cumulative effects on sEMG (i.e., %RMS of the vastus lateralis muscle of right and left legs measured before the first session and before the last session) are shown in Table 7. The vastus lateralis muscle activity was not altered in either leg for either of the groups.

**Table 7.** Cumulative effects on electromyography (%RMS) of vastus lateralis muscle (right and left).


CG: control group; TG: treatment group; SE: standard error; %RMS: percentage of the root mean square; VL: vastus lateralis muscle.

#### **4. Discussion**

All the individuals recruited in the current study presented an increased waist circumference (Table 1); according to the IDF, this is the first criteria followed by a set of two or more metabolic abnormalities to characterize MetS [1].

There is an association between the negative effect of body adiposity and muscle function, with more severe impairment in metabolic disease with IMAT accumulation impacting physical performance [5]. Insulin resistance and type 2 diabetes mellitus are highly prevalent in individuals with MetS [1], and are associated with an infiltration of adipose tissue in skeletal muscles [50]. These features lead to a reduction in the power output and strength per unit of muscle mass. Hilton et al. [51] showed that marked IMAT was inversely correlated with muscle power, strength, and physical performance scores. Lafortuna et al. also reported a negative effect of metabolic abnormalities related to impaired glucose homeostasis on motor performance [52]. IMAT is now recognized as an important predictor of muscle metabolism and function, and also appears to be a modifiable muscle risk factor. Exercise and physical activity appear to be effective countermeasures against increases in IMAT [4]. In addition, exercise is also reported to be an important intervention to improve the physical condition of MetS individuals [26]. Moreover, a simple and useful kind of exercise generated in individuals exposed to mechanical vibration, WBVE, could prove useful for these individuals.

#### *4.1. E*ff*ect of Whole Body Vibration Exercise (WBVE) on Range of Motion (ROM)*

In our study, there was no improvement in knee ROM in individuals with MetS exposed to WBVE. No increase in ROM was observed in a single session or even in a 5-weeks treatment. Our results are in agreement with the findings of Neto et al. (2017), who did not find an increase in ROM in knee flexion in individuals with knee osteoarthritis (KOA) [47]. Wang et al., comparing quadriceps resistance exercise alone and associated with WBVE, observed a significantly greater improvement in active knee flexion and extension at 2 and 4 weeks after quadriceps resistance exercise combined with WBVE in individuals with KOA [53]. Authors have reported that higher body fat is also associated with poor physical performance and subsequent disability than is muscle mass reduction [4,54]. This could justify the results of the current study. In addition, obesity can modify the movements and force response of

these individuals. Del Porto et al. reported that some adaptations of shifts in the body's total ROM are difficult to adjust without compromising normal patterns of movement in obese individuals [55]. Putting together these considerations, it is possible to justify no improvements in the ROM of the knees in the population evaluated in our work. By contrast, Yang et al., in a longitudinal study of 8 weeks with WBVE in individuals with multiple sclerosis, observed a significant increase in the active ROM assessed at the ankle joint bilaterally, in plantar flexion (p = 0.002) and dorsiflexion (p = 0.003). Yang et al. concluded that WBVE increased the flexibility of the ankle joint, reduced the fear of falling, and strengthened the bones [38]. Although Krause et al. observed no changes in the ankle joint excursion immediately after a 1-min bout of WBVE, they found an increase in the knee joint active angular excursion during flexion and extension (p < 0.01) in individuals with cerebral palsy [29]. In another study performed in children with cerebral palsy, a significant increase in ROM was detected immediately after treatment with WBVE [44]. These conflicting results about the effect of WBVE on the ROM of joints could be associated with the variability of the protocols and the populations evaluated.

#### *4.2. E*ff*ect of WBVE on sEMG*

In the present study, significant changes in the electromyographic signal of the VL muscle on both legs were observed in the acute effect of the last session of the 5-week WBVE intervention (Table 6). This is in agreement with other authors that have shown improvement in muscle activity due to WBVE intervention in different muscles in individuals with various diseases [27], such as acute and chronic stroke [30,56], spinal cord injury [24], Friedreich's ataxia [57], and cerebral palsy [29]. Liao et al. detected changes in muscle activity even in individuals with paresis [30]. Furthermore, increased muscular activity was also observed in healthy individuals [34,58]. Borges et al. found that WBVE increased the sEMG amplitude of the VL muscle during an isometric semi-squat exercise in active woman [34]. A systematic review has analyzed the effects of WBVE in lower limbs' neuromuscular activity, suggesting that there was a greater recruitment of motor units after WBVE [27].

In the current study, no effects were observed in %RMS in the acute effect of the first session or in the cumulative effect (Tables 5 and 7). Considering the acute effect, Annino et al. (2017) also reported no alteration in the sEMG of the VL muscle when healthy individuals were exposed to 10 minutes of WBV at 35 Hz [59]. Borges et al. (2016) evaluated the immediate effects of WBV in healthy individuals with frequencies of 30 and 50 Hz, and no significant differences in the value of RMS were found [60]. Considering the cumulative effect (Table 7), the present study found no significant changes in the electromyographic signal of the VL muscle in either leg. Rubio-Arias et al. (2018) also observed no statistically significant differences in body composition or muscle architecture variables, nor changes in muscle activity during the take-off phase of the vastus lateralis pre- versus post-training in a 6-week WBVE treatment with a frequency between 30 and 45 Hz in healthy individuals [61].

Some limitations of this study should be pointed out, such as the relatively small number of participants; however, the statistical power was 95 %. Moreover, although we evaluated both lower limbs, we did not register which lower limb was the dominant one. Nevertheless, a strength of this work is the improvement in neuromuscular activity; this finding may have positive clinical implications by improving daily activities in individuals with MetS.

In conclusion, WBVE can be a modality of exercise to increase the neuromuscular activity of the VL muscle using a 5-week protocol. An increase in ROM of the knees in individuals with MetS was not observed with the same protocol. WBVE appears to be an adequate strategy to improve neuromuscular activity in individuals with MetS, overweight, and obesity, being a potential opportunity for the management of physical impairment in these individuals. Nevertheless, further additional studies with larger samples and more prolonged periods of WBVE exposure are needed to confirm our preliminary findings.

**Author Contributions:** Conceptualization, M.B.-F.; Data curation, C.R.d.S.-G., D.d.C.d.S.-C., L.L.P.-D., E.M.-M., M.E.S.M.-O., Y.T.-S., A.P.d.S.L., J.A.B., M.J.d.S.P., V.L.X., A.G.d.M., L.F.F.D.S., A.R.-S., A.F.-S., G.M.G.-L., M.C.M.-F., A.d.R.P.M., T.A., A.C.R.L., V.A.M., A.S. and M.B.-F.; Formal analysis, M.J.d.S.P., V.L.X., and R.T.; Funding

acquisition, M.B.-F.; Investigation, C.R.d.S.-G., D.d.C.d.S.-C., L.L.P.-D., E.M.-M., M.E.S.M.-O., Y.T.-S., A.P.d.S.L., A.G.d.M., L.F.F.D.S., A.R.-S., A.F.-S., G.M.G.-L., M.C.M.-F. and A.d.R.P.M.; Methodology, C.R.d.S.-G., D.d.C.d.S.-C., L.L.P.-D., E.M.-M., M.E.S.M.-O., Y.T.-S., A.P.d.S.L., A.G.d.M., L.F.F.D.S., A.R.-S., A.F.-S., G.M.G.-L., M.C.M.-F. and A.d.R.P.M.; Supervision, D.d.C.d.S.-C.; Writing—original draft, C.R.d.S.-G. and Y.T.-S.; Writing—review & editing, D.d.C.d.S.-C., J.A.B., R.T., T.A., A.C.R.L., V.A.M., A.S. and M.B.-F.

**Funding:** This research was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)—Finance Code 001, and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

**Acknowledgments:** The authors are grateful for the support of the Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)—Finance Code 001, and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

**Conflicts of Interest:** The authors declare that there is no conflict of interests regarding the publication of this paper.

#### **Abbreviations**


#### **References**


© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).

### *Article* **Test-Retest Reliability of Kinematic Parameters of Timed Up and Go in People with Type 2 Diabetes**

**Francisco J. Dominguez-Muñoz 1, Miguel A. Hernández-Mocholi 1, Luis J. Manso 2, Daniel Collado-Mateo 3,\*, Santos Villafaina 1,\*, Jose C. Adsuar <sup>4</sup> and Narcis Gusi 1,5**


Received: 13 September 2019; Accepted: 1 November 2019; Published: 5 November 2019 -

**Abstract:** Diabetes mellitus is a chronic disease defined as a state of hyperglycaemia in fasting or postprandial states. Patients with type 2 diabetes mellitus (T2DM) often show reduced physical function, including low levels of strength, balance or mobility. In this regard, the timed up and go (TUG) is a widely used physical fitness test in people with T2DM. However, there is a lack of studies evaluating the properties TUG in this population. The present study aimed to evaluate the test-retest reliability of kinetic and kinematic parameters obtained from TUG in the diabetic population with different levels of diabetic neuropathy. A total of 56 patients with T2DM participated in the study. They were divided into three groups according to the vibration threshold: (a) severe neuropathy, (b) moderate neuropathy and (c) normal perception. The TUG was performed using two force platforms to assess kinematic measurements. The results show that both kinetic and kinematic variables had good to excellent reliability. The reliability of TUG was excellent for the whole sample and the groups with non-severe neuropathy. However, it was just good for the group with severe neuropathy.

**Keywords:** forefoot; Gait; Heel; TUG; Type 2 diabetes mellitus

#### **1. Introduction**

Diabetes mellitus (DM) is a chronic disease defined as a state of hyperglycaemia in fasting or postprandial states [1]. DM is one of the largest global public health problems and affects approximately 415 million people in the world among adults aged 20–79 years-old. It is estimated that, in the year 2040, there will be 642 million persons (confidence interval 521–829 million) with DM in the world [2]. The International Diabetes Federation also estimates that, globally, 46.5% of people suffering from diabetes were still undiagnosed in 2015, which may markedly increase the reported prevalence. According with the American Diabetes Association (ADA), the total costs for diabetes care in the United States were approximately 245 billion dollars due to medical costs, lost productivity and disability [3]. Much of the burden of this disease comes from vascular complications, which include cardiovascular disease, retinopathy and nephropathy. Another complication is diabetic peripheral neuropathy, affecting more than 50% of long-term diabetic cases [4].

Diabetic neuropathy is characterised by progressive degeneration that primarily affects small-diameter cutaneous nociceptive fibres [5]. It may also affect motor fibres, which can cause muscular weakness. In this regard, persons with DM have a reduction of 17% and 14% in the strength of the flexor and extensor muscles of the knee, respectively [6]. Somatosensory feedback is a relevant factor to maintain balance and there is strong evidence showing that diabetic neuropathy affects this source of information, leading to alterations in postural and gait performance [7]. In this regard, previous studies have demonstrated that the main sources of deterioration in the balance in persons with type 2 DM (T2DM) are deficits in the proprioception of the foot and the ankle [8], or a loss of sensitivity in the feet [9].

The neurologic exam of the lower limb is the most important aspect in the clinical diagnosis of diabetic neuropathy [10]. The loss of foot vibration perception is associated with an increased risk of foot ulceration in people with diabetes [11]. In this regard, Abbott et al. [12] showed that each one-unit increment in the foot vibration threshold increases the risk of foot ulceration by more than 5% in a single year period. Therefore, the foot vibration threshold is a very relevant variable in the diabetic population.

Previous studies have demonstrated a relationship between the foot vibration threshold and the risk of falling [13], gait speed [14] and mobility disability [15]. Although balance and mobility tests are of great interest in DM studies due to the association with the risk of falling and the ability to perform activities of daily living, a recent systematic review showed that there is a lack of studies evaluating the properties of these tests when they are conducted in the diabetic population [16].

Therefore, the main objective of this study was to evaluate the test-retest reliability of the kinetic and kinematic parameters obtained from one of the most widely used tests for assessing balance and mobility, the timed up and go (TUG), in people suffering from T2DM. The second objective was to calculate the reliability of TUG according to the severity of peripheral neuropathy (assessed through an evaluation of the foot vibration threshold).

#### **2. Materials and Methods**

#### *2.1. Participants*

A total of 56 patients with DM participated in the study. Of these, 40 were men and 16 were women. The following inclusion criteria were: (a) diagnosed with T2DM, (b) affected by at least one risk factor of diabetic neuropathy: (1) being overweight, (2) a former smoker, (3) diagnosed with diabetic nephropathy and (4) diagnosed with diabetic retinopathy, (c) levels of glycated haemoglobin higher than 5.7%, and (d) have read and signed the written informed consent. In addition to these inclusion criteria, some exclusion criteria were defined: (a) pregnancy, (b) the use of psychotropic or chemotherapeutic medications, (c) affected by other diseases that may influence balance and gait, such as Parkinson's disease, and (d) patients with a high risk of non-diabetic neuropathy (HIV or uraemia). The protocol of the present study was approved by the Committee of Bioethics of the University and was developed in accordance with the updated Helsinki Declaration and the national legislation on bioethics, biomedical research and personal data confidentiality.

#### *2.2. Procedure*

After reading and signing the written informed consent, participants were measured and weighed. They were also asked about their age and years since diagnosis. Then, the vibration threshold was evaluated and, finally, the TUG was conducted after a light warm-up.

The foot vibration threshold was assessed using a Biothensiometer Vibratron II (Physitemp Instruments, Inc. Clifton; New Jersey; USA). This device drives vibration to modules A and B placed under the feet of the participant. Each module has a vibrating pole on the top, which vibrates at a frequency of 120 Hz. Therefore, the vibration threshold is determined by modifying the amplitude. These vibration units are related to the amplitude of the movement in microns according to the formula:

*A* = *x*2/*2* (where x is the vibration units (vu) and A is the amplitude in microns (μm)). The present study used the protocol the 'force two alternative choices procedure', which is one of the two methods suggested by the manufacturer. Participants were asked to place their first toe on the vibrating pole. The procedure started when the participant felt the vibration in the left or right toe. After that, the amplitude was reduced progressively until the participant was not able to tell which pole was vibrating. When the participant failed to detect vibration, the amplitude of the vibration was increased. The vibration threshold was then calculated using the last five rights and wrongs, but omitting the extreme low and high values. The average of the remaining eight values was then computed to calculate the vibration threshold [17].

TUG was performed three times, with a 5-min rest in between. The first repetition was for familiarisation, the second was the test measure and the third was the retest measure. All participants performed a light warm-up which included walking and joint mobility for 5 min. In the TUG, two force platforms (Kistler, NY, USA) were placed between the chair and the mark where participants had to turn around. Therefore, participants stepped on the platforms before and after reaching the mark placed at 3 m. The time required to complete the full test was assessed manually with a stopwatch by an expert rater.

Variables obtained from the force platforms included the duration of (a) the double support phase (both feet on the platforms), (b) left support (only the left foot on the platforms) and (c) right support (only the right foot on the platforms), as well as the left and right peak forces from the forefoot and the heel.

The results are presented for the whole sample (*n* = 56), and also according to the degree of neuropathy based on vibration perception, i.e., severe neuropathy (*n* = 22), moderate neuropathy (*n* = 22) and normal perception (*n* = 12). To classify patients into one of the three groups, the cut-off points suggested by normative values of the manual of the measuring device were considered.

#### *2.3. Statistical Analysis*

Descriptive statistics included mean and standard deviation (SD) of age, weight, glycated haemoglobin, years since T2DM diagnosis, body mass index and vibration threshold were calculated for the whole sample and divided into women or men. Parametric and non-parametric tests were conducted based on the results of Shapiro-Wilk and Kolmogorov-Smirnov tests.

Differences between test and retest were evaluated using the paired samples t-test or Wilcoxon signed rank test when appropriate. The time spent to complete the TUG, the duration of phases and the forces registered by the force platforms were included in those analyses to compare the test and retest results.

Reliability analyses were conducted in accordance with the recommendations of Weir [18]. An intraclass correlation coefficient (ICC) of 3.1 (two-way mixed, single measures) with a 95% CI for test and retest [19] was selected. Both absolute and relative reliability were computed. The standard error of measurement (SEM) was calculated as *SEM* <sup>=</sup> *SD* <sup>√</sup> 1 − *ICC* where SD is the mean SD of the three repetitions, while the smallest real difference (SRD) was *SRD* <sup>=</sup> 1.96 <sup>×</sup> *SEM* <sup>×</sup> <sup>√</sup> 2. These measures were converted into percentages (%SEM and %SRD, respectively) to enable comparisons with other investigations.

#### **3. Results**

#### *3.1. Participant Characteristics*

Table 1 summarises the participant characteristics. A total of 40 men and 16 women aged 64.52 (8.41) and 67.43 (8.86), respectively, participated in the present study. The mean weight of the whole sample was 80.08 (17.59) kg and the body mass index (BMI) was 28.81 (4.40) kg/m2. The mean vibration threshold was 4.27 (1.90) for women and 5.75 (2.50) for men.


**Table 1.** Participant characteristics.

BMI: body mass index; vu: vibration units.

#### *3.2. Kinematic Variables of the Timed Up and Go*

Table 2 summarises the mean duration of the walking phases in the TUG. The results from the paired samples *t*-test or Wilcoxon signed rank test showed that there were significant differences between the test and retest values in some of the variables, including the time required to complete the TUG and the duration of the left support before reaching the mark for the whole sample. These differences were also observed in the group with severe neuropathy.



<sup>a</sup> *p*-values obtained from the Wilcoxon signed rank test.

Reliability parameters for the total time required to complete the TUG and duration of phases can be observed in Table 3. The ICC was good (0.70 to 0.90) or excellent (>0.90) for almost every variable and group. The best reliability was obtained for the time required to complete the TUG, which was excellent in the two groups with non-severe neuropathy, while it was just good in the group with severe neuropathy.



#### *3.3. Peak Forces from the Heel and the Forefoot in the Timed Up and Go*

Regarding the peak forces from the heel and the forefoot, differences between test and retest were only observed for the right heel and left forefoot forces in the group without neuropathy. For the rest of the variables, the retest was not significantly different than the test (see Table 4).

**Table 4.** Differences between the test and retest on the peak forces from the heel and the forefoot forces in the entire sample and in participants with (a) severe neuropathy, (b) moderate neuropathy and (c) normal perception.



**Table 4.** *Cont*.

<sup>a</sup> *p*-values obtained from the Wilcoxon signed rank test.

Table 5 summarises the reliability analyses of the kinetic variables for the whole sample and according to the neuropathy classification. Reliability was excellent (ICC > 0.90) in almost every variable and group, except for the left forefoot forces after reaching the mark in the group with normal vibration perception.



#### **4. Discussion**

The present study aimed to evaluate the test-retest reliability of kinetic and kinematic parameters obtained from TUG in the diabetic population. The results were analysed according to the severity of neuropathy. The main finding was that almost each variable achieved good (ICC between 0.70 and 0.90) or excellent (>0.90) reliability considering the classification by Munro et al. [20].

The reliability of TUG seemed to be conditioned by the severity of neuropathy since the ICC was higher than 0.90 (excellent) for participants with moderate neuropathy and patients with normal foot vibration perception, but just good (0.70 to 0.90) for patients with severe neuropathy. Therefore, although the TUG is reliable in T2DM patients, changes in the duration of the phases (single and double support) must be taken with caution since the %SEM may be relatively high in some cases (over 10%). Furthermore, we can observe how the SRD of the required time to complete the TUG was higher in patients with severe neuropathy. These results must be considered by clinicians and researchers in order to interpret their results when using TUG in the T2DM population. This is relevant since a previous study showed that patients with diabetic neuropathy have worse health-related quality of life and lower functional status than patients without diabetic neuropathy [21]. Neuropathy leads to balance impairments [22], gait and mobility alterations [23,24] and an increased risk of falls [25]. In addition, patients with T2DM seem to be more susceptible to falls and consequently to bone fractures [26–28]. Due to the relevance of diabetic neuropathy in patients with T2DM, future studies aimed at improving physical conditioning variables should consider that the smallest clinically relevant improvement may be higher in T2DM patients with this complication.

To our knowledge, this is the first study to assess the reliability of TUG according to the severity of neuropathy. Only one previous study has evaluated the reliability of TUG in the diabetic population [29]. That study was conducted on a sample of 18 older adults with T2DM, and no classification of the participants was performed. Furthermore, that study only evaluated the time needed to complete the TUG and not any other measure such as the duration of walking phases or kinetic parameters. Comparing results from the present study with those obtained by Alfonso-Rosa, Del Pozo-Cruz, Del Pozo-Cruz, Sanudo and Rogers [29], both studies report excellent reliability. However, the ICC and %SEM from that study were 0.98 and 3.5%, respectively, whereas the present study reports an ICC of 0.927 and a %SEM of 4.52. Therefore, the reliability is slightly lower in this study, which may be linked to the greater heterogeneity of the sample in the current study. In this regard, it must be noted that the study by Alfonso-Rosa, Del Pozo-Cruz, Del Pozo-Cruz, Sanudo and Rogers [29] was conducted on 18 older adults with T2DM, while the current one was conducted with 56 adults aged 65.35 (8.56) years.

The current study reported not only the SEM but also the SRD, which is extremely relevant for clinicians and researchers since it indicates whether the differences obtained as a consequence of an intervention program could be considered clinically important [30]. A previous study in T2DM [29] established the SRD for the TUG at 9.8%, whereas in the present study the SRD was 12.55%. This difference could be also explained by the heterogeneity of the sample in the current study. In this regard, the results from the previous study were limited to older adults. Thus, those studies conducted with samples comprised of adults (but not limited older adults) had no information about the reliability and the minimal clinically important difference to interpret their results. Therefore, the current study was needed since it is the first to provide reliability information in a sample comprised of adults (not limited to older adults).

Test-retest analyses have been also reported in kinematic parameters, taking into account the heel and the forefoot forces during the TUG. The results revealed that the reliability of the heel and forefoot forces could be considered as excellent, so future studies can confidently use this as a measurement to evaluate gait patterns in T2DM patients. People with diabetic neuropathy often have balance problems while performing common activities such as walking or ascending/descending stairs [31]. Furthermore, the postural mechanisms at the ankle joints are impaired in diabetic neuropathy patients during quiet standing [32]. Thus, postural instability and gait imbalance in diabetic neuropathy may contribute to a high risk of fall incidence, especially in the geriatric population [7,31]. Therefore, future studies should be focused on the implementation of interventions aimed to modify gait parameters to reduce the risk of falling in T2DM patients. The current study provides useful information in order to interpret

changes achieved after a specific program, stating the minimal clinically relevant change for kinetic and kinematic variables.

The present study has two main limitations. First, although the sample size (*n* = 56) was sufficient to conduct this test-retest reliability analysis, the group with no alteration in the foot vibration threshold was comprised of only 12 people. The second limitation may be related to the inclusion criteria and the difficulty in determining that peripheral neuropathy is caused by diabetes. Even though the inclusion and exclusion criteria were very restrictive (excluding people with other diseases and people who were taking drugs that may potentially affect balance and gait), there could be other non-diagnosed diseases, environmental factors or healthy/unhealthy habits that may increase or reduce neuropathy. In spite of these two limitations, this study succeeded at reporting reliability parameters according to the severity of neuropathy in patients with T2DM.

#### **5. Conclusions**

The reliability of TUG was excellent for the whole sample and the groups with non-severe neuropathy. However, it was just good for the group with severe neuropathy. Regarding the kinetic and kinematic parameters, the reliability was good or excellent for almost every variable and group. The present study reports the minimal change that may be considered real (SRD) and the SEM, which should be considered by future studies aimed to assess the effects of interventions on different variables related to the TUG.

**Author Contributions:** F.J.D.-M., J.C.A., M.A.H.-M. conceived the study. F.J.D.-M., S.V. and D.C.-M. collected the data. F.J.D.-M., N.G., L.J.M., D.C.-M. analysed the data. S.V., N.G. and D.C.-M. designed the figures and tables. F.J.D.-M., J.C.A. and D.C.-M. wrote the manuscript. S.V., M.A.H.-M., L.J.M., and N.G. provided critical revisions on successive drafts. All authors approved the manuscript in its final form.

**Acknowledgments:** The author SV is supported by a grant from the regional Department of Economy and Infrastructure of the Government of Extremadura and European Social Fund (PD16008). We are grateful to the Primary Care Centre "Manuel Encinas" in Cáceres for helping recruit the participants for this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

**Conflicts of Interest:** The authors declare no competing interests.

#### **Abbreviations**


SRD Smallest real difference

#### **References**


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#### *Article*
