*Article* **Postural Instability after Stepping on a Stair in Older Adults: A Pilot Study**

**Hyokeun Lee <sup>1</sup> and Kyungseok Byun 1,2,\***


**\*** Correspondence: vbiomechanics@gmail.com; Tel.: +82-10-2876-3815

**Abstract:** This study aimed to examine how older adults (OA) control their postural stability after stepping on a stair in comparison to young adults (YA). Ten OA and 10 YA participated in this study. Participants ascended a single stair (15 cm high by 30 cm wide) which was secured atop one of the force plates. Ground reaction forces (GRFs) and center of pressure (COP) motion data were obtained from the force plate under the stair. After standing on the stair with both feet, GRFs and COP data for a 3 s duration were analyzed to assess postural variables, including time to stabilization (TTS), COP velocity (COPVEL), and COP sway area (COPSWAY). A significant difference in TTS in the anterior–posterior direction between OA and YA (*p* = 0.032) was observed, indicating that OA had difficulty stabilizing their body posture after the stair ascent compared to YA. For COP postural variables, no significant differences in COPVEL (*p* = 0.455) and COPSWAY (*p* = 0.176) were observed between OA and YA. Study findings indicate that older adults have less capacity to regain postural stability compared to young adults following a challenging dynamic movement.

**Keywords:** postural stability; older adults; stepping on a stair; time to stabilization

Instability after Stepping on a Stair in Older Adults: A Pilot Study. *Appl. Sci.*

Academic Editor: Nyeonju Kang

**2021**, *11*, 11885. https://doi.org/ 10.3390/app112411885

**Citation:** Lee, H.; Byun, K. Postural

Received: 28 October 2021 Accepted: 13 December 2021 Published: 14 December 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 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 (https:// creativecommons.org/licenses/by/ 4.0/).

#### **1. Introduction**

Postural instability in older adults (OA) leads to impaired balance control when performing activities of daily living, potentially causing an increased risk and incidence of falls and a reduction of independence and quality of life [1]. Given that the biomechanical mechanisms of postural instability in OA have been well documented [2], the balance deficits of OA have been shown to manifest not only during static movements [3], but also during dynamic transitive movement in daily activities [4].

A stair ascent task is a functionally relevant motor task that significantly challenges the locomotor and postural control system. Biomechanically, stair ascent requires significant momentum, which is necessary for conjoint upward and forward body propulsion [5]. Indeed, stabilizing one's body posture following stair ascent is needed to offset the propulsive momentum generated by the whole body. Accordingly, individuals with strength deficits may be more impaired at controlling stability after a stair ascent task, exhibiting alterations in their strength compensation strategy. Indeed, it has been reported that individuals with muscular and neurologic deficits (e.g., osteoarthritis and stroke) are at a greater risk of having a stepping-related fall due to biomechanical and environmental constraints [6,7].

When comparing OA and YA (young adults), OA are at higher risk of loss of balance and falls during stair ascent in comparison to YA, in part due to muscular deficits. Specifically, muscle weakness in the elderly causes abnormal gait patterns and changes their gait biomechanics, particularly affecting gait velocity, and with less strength in their lower extremities leading to their greater incidence of falls [8,9]. Despite greater predicted possibilities that OA show balance problems and falls, studies have thus far focused less on motor control in dynamic activities, such as stepping up stairs, and even less on comparatively examining OA and YA.

Additionally, stair ascent is a complex task that is cognitively demanding compared to other simple tasks (e.g., sit-to-stand) [10], and age differences in cognitive abilities have been clearly shown [11]. A study proposed that significantly more attentional resources are required during stair ascent in OA than YA, while greater attentional resources are not required during simple tasks, such as standing [12]. It is also highlighted that cognitive decline is a common problem observed in the elderly [13]. Thus, stair ascent task assessments provide important insights into biomechanical abilities that cannot be captured through simple tasks for OA, while being sensitive to different cognitive abilities by age.

The purpose of the current study was to examine how stabilizing capabilities after stepping up stairs in OA faired in comparison to YA, hypothesizing that OA would take longer to stabilize their body posture and would have less ability to regain static plateau after the stepping performance. To find the exact time point at which one's postural sway is in plateau, we utilized the 'time to stabilization (TTS)' metric, which provides underlying information calculated based on overall information in a time series. It is useful and applicable when assessing dynamic balance capability.

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

#### *2.1. Participants*

Ten OA (Age: 71 ± 4.2 yr, height: 170.6 ± 5.4 cm, body mass: 73.2 ± 9.4 kg) and 10 YA (age: 27 ± 6 yr, height: 172.1 ± 7.4 cm, body mass: 72.5 ± 13.8 kg) participated in this study. All participants were asked to perform a cognition test (the mini-mental state examination, or MMSE) for screening purposes, and those who obtained a score of 23 or under were excluded from participating in the study. Participants had not had any musculoskeletal problems within the past six months and had not had any recent surgery. Informed consent was reviewed with each participant, and once all questions were answered and the documentation of consent was obtained, the experimental session began.

#### *2.2. Experimental Protocol*

Sixteen passive reflective markers were attached to the lower body in accordance with the instructions that accompanied the Helen Hays marker set, and kinematic data were collected using a 10-camera motion capture system (100 Hz, Qualisys, Gothenburg, Sweden). For the stair ascent trial, participants ascended a single stair (18 cm high by 40 cm wide), which was secured atop one of the force plates, barefoot. In response to a verbal signal of "ready", participants were asked to wait a moment and then begin the movement by stepping onto the stair with their dominant leg and maintain their stability (for at least 5 s) in a static position once both feet were atop the stair. Further, during the stepping task, participants were asked to fold their arms across their chest. The events of the stepping performance, including (1) the initial foot being raised from the ground, (2) the initial foot making contact with the stair, (3) the second foot being raised from the ground, and (4) the second foot making contact with the stair, were identified based on the ground reaction force data and the feet kinematic data. Ground reaction forces (GRFs) and moments were recorded using two force plates, one mounted on the laboratory floor and the other on the stair (300 Hz, Kistler, Winterthur, Swiss) (Figure 1). We measured GRFs and center of pressure (COP) motion along the anterior–posterior (AP) and mediolateral (ML) axes of motion for data analysis, and filtered GRF and COP data using a second-order Butterworth low-pass filter with a cutoff frequency of 5 Hz. GRFs and COP data were captured for a duration of 3 s after both feet were standing on the stair to assess the subjects' postural stabilization.

**Figure 1.** Experimental protocol of the stepping on a stair task with two force plates, one mounted on the laboratory floor (the first plate) and the other on the stair (the second plate).

#### *2.3. Data Reduction and Processing*

We obtained GRF and center of pressure (COP) motion data along the anterior– posterior (AP) and medial–lateral (ML) axes of motion for data analysis, and filtered the GRF and COP data using a second-order Butterworth low-pass filter with a cutoff frequency of 5 Hz. GRFs and COP data were measured for a duration of 3 s after both feet were standing on the stair (event four: when the second foot came into contact with the stair) to assess the subjects' postural stabilization.

Time to stabilization (TTS) scores for the AP and ML directions were separately calculated according to the ground reaction forces (x vector, AP; y vector, ML). As a sequential estimation, TTS incorporates an algorithm to calculate a cumulative average of the data points in a series by successively adding one point at a time [14]. This cumulative average value is sequentially compared with the overall series mean. When the value of the sequential average passes through a level that is within 0.25 SDs of the overall series mean, the individual series is considered to be at a plateau stage. The series consists of all data points within the first 3 s of both feet making contact with the stair (Figure 2).

**Figure 2.** Time to stabilization in OA and YA calculated using ground reaction forces measure-ments.

For the traditional postural assessment, we also calculated COP velocity (COPVEL) and sway of 95% confidence ellipse (COPSWAY), which were calculated around the filtered COP motion along both the AP and ML axes (Figure 3). The details regarding the procedure to calculate COPVEL and the COPSWAY are described in previous literature [15,16].

**Figure 3.** The center of pressure (COP) trajectories during posture stabilization after a stepping movement in OA and YA.

#### *2.4. Statistical Analysis*

Descriptive statistics for age, body mass, height, and MMSE were calculated for both groups. Independent *t*-tests were used to compare all dependent variables between OA and YA. Statistical analyses were performed using SPSS, and all levels of significance were set at α = 0.05.

#### **3. Results**

A significant difference in TTS AP between OA and YA (*p* = 0.032) and a marginal but not statistical difference in TTS ML (*p* = 0.141) were observed, indicating that OA needed a longer time to stabilize their body posture after stair ascent compared to YA. For COP postural variables, no significant difference in COPVEL (*p* = 0.455) and COPSWAY (*p* = 0.176) were observed between OA and YA (Table 1).

**Table 1.** Mean, standard deviation, and *p*-value from *t*-tests for all dependent variables, including TTS AP, TTS ML, COPVEL, and COPSWAY. *p* < 0.05 for difference between OA and YA.


\* Significant difference between OA and YA at *p* < 0.05.

#### **4. Discussion**

There have been only a few studies using time to stabilization (TTS) to assess postural capacity in older adults (OA) or disease populations. A previous study utilized TTS to assess how stroke patients control their postural stability in response to unpredicted perturbation [17]. They reported that stroke patients who had intensive weighted training showed decreased TTS scores, indicating their improved capacity to stabilize their postural sway in the face of unpredicted perturbations. Bieryla and Madigan [18] further demonstrated that an improvement in one's postural stability as measured by TTS was observed more in older adults who had exercise training than those without training.

To our knowledge, this preliminary investigation is the first to assess the stabilization capacity of OA following a stepping movement, as measured by TTS. There have been a few studies that have compared spatiotemporal measures and the stabilizing strategies of OA and YA during stair ascent. One study reported that there were no significant group differences in stepping performance [19], while another study reported that OA show smaller separations between the center of mass and the center of pressure, which is indicative of different stepping strategies between groups [20]. However, no study examined the stabilization capacity after the stepping movement had been completed. By using TTS in this study, we tried to account for the deficits of stabilizing capacity in OA during a challenging dynamic movement. As hypothesized, OA exhibited a significantly longer time to stabilize their postural sway following stair ascent in comparison to YA. This finding indicated that OA may have less capacity to regain postural stability compared to YA following a challenging task, such as stepping on a stair. Given that a longer time for stabilization is highly correlated with a greater risk of falls [21], our TTS finding supports the observation that OA are at a greater risk of falls compared to YA. The finding of the current study could potentially provide a reliable and objective index for the evaluation of dynamic postural stability in OA.

However, we did not observe any significant differences between OA and YA in balance performance during posture stabilization after stepping on a stair when we assessed this using COP measures (e.g., COPVEL and COPSWAY). Conventionally, balance problems in OA have been identified by evaluating the COP motion [22]. For example, greater velocity or sway area during static movement has been considered to be one of the representative characteristics of postural control deficits in OA [23]. Biomechanically, however, dynamic movement, such as stair ascent, require a sufficient level of body momentum and co-contraction between COP and the body's center of mass to maintain postural stability when compensating for propulsive body momentum [24]. Unlike static standing, such dynamic movements are likely performed with greater variation because the majority of factors (e.g., force generation, cognition, and the environment itself) are consistently working as determining contributors to overall dynamic performance [25]. Therefore, it is difficult to account for postural capacity by using traditional COP measures, such as sway area or velocity, when biomechanically investigating dynamic balance.

There were limitations to the current pilot study. In a previous biomechanical study measuring TTS in athlete populations, it was reported that ankle joint stability, braces, and fatigue were closely related to TTS, indicating that ankle joint functions play a crucial role in dynamic balance and time to stabilization when experiencing an external perturbation [26]. Although previous studies investigated the balance recovery function using the TTS measure, which is consistent with our investigation, results from the current study should be interpreted with careful consideration. Particularly, unlike a previous study [27], subjects in our investigation were screened out when they had any musculoskeletal problems and fatigue. Therefore, we speculate that there might be other factors that affect TTS scores (e.g., muscle strength), which clearly differentiated the balance recovery functions between OA and YA.

#### **5. Conclusions**

The findings in this study will have the potential to give us a better understanding of how the elderly experience postural instability in daily life. More research is needed, however, to confirm the current findings and expand our understanding of what constitutes meaningful biomechanical change according to TTS scores in OA. The capability to stabilize one's posture after completing a dynamic movement is primarily based on how a person negotiates various physical constraints that result from neuroanatomical, biomechanical, and environmental origins. Thus, to better understand the neuromuscular system underlying postural control recovery strategies in OA, diverse factors, such as muscle power and psychiatric aspects (e.g., fear of falling), on postural control should be comprehensively considered in future studies.

**Author Contributions:** Conceptualization, H.L.; methodology, H.L.; writing—original draft preparation, H.L.; writing—review and editing, H.L. and K.B.; supervision, K.B.; project administration, H.L. and K.B. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.

**Institutional Review Board Statement:** The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Institutional Review Board of the University of Florida (IRB201401029).

**Informed Consent Statement:** Informed consent was obtained from all participants involved in the study.

**Data Availability Statement:** Not applicable.

**Acknowledgments:** We thank the study participants for their time and effort.

**Conflicts of Interest:** The authors declare no conflict of interest.

#### **References**


**Jin-Su Kim 1, Moon-Hyon Hwang 1,2 and Nyeonju Kang 1,3,4,\***


**Abstract:** The purpose of this study was to investigate bilateral deficit patterns during maximal handgrip force production in late postmenopausal women. Twenty late postmenopausal and 20 young premenopausal women performed maximal isometric grip force production tasks with dominant and nondominant hands and both hands, respectively. For late postmenopausal women, pulse wave analysis was used for identifying a potential relationship between maximal hand-grip strength and risk factors of cardiovascular disease. The findings showed that late postmenopausal women produced significantly decreased maximal hand-grip strength in dominant and nondominant and bilateral hand conditions compared to those of premenopausal women. Bilateral deficit patterns appeared in late postmenopausal women. For late postmenopausal women, decreased dominant and bilateral hand-grip forces were significantly related to greater bilateral deficit patterns. Further, less maximal hand-grip strength in unilateral and bilateral hand conditions correlated with greater central pulse pressure. These findings suggested that age-related impairments in muscle strength and estrogen deficiency may interfere with conducting successful activities of bilateral movements. Further, assessing maximal dominant hand-grip strength may predict bilateral deficit patterns and risk of cardiovascular disease in late postmenopausal women.

**Keywords:** bilateral deficit; postmenopausal; hand-grip strength; dominant hand; pulse wave analysis

#### **1. Introduction**

Menopause typically occurs in women's 40s [1], and one third of women's lifespan is spent post-menopause [2]. Progressive reduction of estrogen in postmenopausal women may facilitate more age-related deficits in the central and peripheral nervous system [3–6]. For example, muscle weakness normally appears in elderly people because of age-induced neurophysiological alterations [7–9]. Furthermore, asymmetrical interlimb muscle strength interferes with executing bilateral movements that account for 54% of daily activities in the aging population [10,11]. Importantly, postmenopausal women reveal more significant reduction of muscle strength than premenopausal women and age-matched males [12–16].

Bilateral deficit is a phenomenon when individuals reveal lower force outputs produced simultaneously by both limbs than the sum of unilateral forces generated by each limb. Previous studies indicate that bilateral deficit may appear in either upper or lower extremities during various motor tasks such as maximal voluntary contraction (MVC), reaction time [17–19], and different contraction types (e.g., isometric and dynamic contraction) [20]. Moreover, greater levels of bilateral deficit are associated with increased impairment in bilateral performances (e.g., ballistic push-off and vertical squat jumping) [21–23], and several aging studies report bilateral deficit patterns in elderly people interfering with various functional movements (e.g., rising from a chair) [24,25].

**Citation:** Kim, J.-S.; Hwang, M.-H.; Kang, N. Bilateral Deficits during Maximal Grip Force Production in Late Postmenopausal Women. *Appl. Sci.* **2021**, *11*, 8426. https://doi.org/ 10.3390/app11188426

Academic Editor: Mark King

Received: 18 August 2021 Accepted: 8 September 2021 Published: 10 September 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 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 (https:// creativecommons.org/licenses/by/ 4.0/).

For postmenopausal and elderly women, previous studies report bilateral deficit patterns in lower limb movements such as leg extension and leg press [24–28]. Specifically, greater bilateral deficit in producing explosive forces increases the time of sit-to-stand performance [25]. In postmenopausal women, increased interhemispheric inhibition and reduced muscle strength potentially induced by deficiency of estrogen and/or progesterone may facilitate bilateral deficit patterns [20,28,29]. However, these previous findings are mostly limited to lower limb movements. Given that successful bilateral upper limb movements are additional critical motor functions for older adults [11], determining whether bilateral deficit patterns in upper limb movements appear in late postmenopausal women is necessary. Thus, the purpose of this study was to examine bilateral deficit patterns in late postmenopausal women using voluntary maximal handgrip force tasks.

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

#### *2.1. Particiapants*

Twenty healthy late postmenopausal women (mean and standard deviation of age = 65.5 ± 3.1 years) and 20 healthy young premenopausal women (mean and standard deviation of age = 23.4 ± 2.1 years) participated in this study. We recruited participants using flyers in the university and local community centers and confirmed that all participants had no musculoskeletal deficits (e.g., sarcopenia) in their upper extremities, neurological disease, cardiovascular diseases, and significant cognitive impairments. Late postmenopausal women were defined as those with more than four years after menopause [30]. All participants were right-handed as assessed by the Edinburgh handedness inventory [31]. Specific details on demographic information are summarized in Table 1. Before starting the testing, all participants read and signed an informed consent form and experimental protocols approved by the University's Institutional Review Board.



Note. Data are mean ± standard deviation. Age data are median (interquartile range).

#### *2.2. Experimental Setup*

To investigate the bilateral deficit phenomenon in the upper extremities, we used an isometric hand-grip force production paradigm. Before executing isometric force production tasks, participants sat 80 cm away from a 54.6 cm LED monitor (1920 × 1080 pixels; refresh rate = 60 Hz, Dell, Round Rock, TX, USA) and maintained comfortable positions with 15–20◦ of shoulder flexion and 20–45◦ of elbow flexion. Using an isometric hand-grip force measurement system (SEED TECH Co., Ltd., Bucheon, Korea), participants grasped the handle (diameter = 30 mm) and produced their maximal isometric force outputs with their unilateral hand and both hands, respectively. Further, we instructed the participants to put their resting hand on the pad during the unilateral tasks and maintain their forearms fixed on the table with same position to avoid inadvertent force output caused by elbow, shoulder, or trunk movements.

We administered two consecutive maximal force production trials for each hand condition: (a) unilateral dominant hand (Figure 1a), (b) unilateral nondominant hand (Figure 1b), and (c) both hands (Figure 1c). For each trial, participants generated as much isometric hand-grip forces as possible for 3 s. They had 60 s of rest between trials and 180 s of rest between hand conditions. The mean of two maximal force production trials for each hand condition was used for further analysis.

**Figure 1.** Hand-grip force production task. (**a**) Unilateral dominant hand contraction, (**b**) Unilateral nondominant hand contraction, and (**c**) Bilateral hands contraction.

Changes in handgrip strength in the aging population may be a risk factor indicating the occurrences of various cardiovascular diseases (e.g., hypertension, coronary artery disease, heart failure, or stroke) [32,33], and reduction of handgrip strength in elderly women is highly related to all-cause mortality [34]. Thus, for late postmenopausal women, we additionally performed non-invasive pulse wave analysis (PWA) using the SphygmoCor Xcel system (AtCor Medical, Sydney, Australia) to investigate the potential relationship between hand-grip force productions and cardiovascular disease risk factors. Before the PWA data collection, participants fasted for at least 10–12 h. All measurements proceeded in a light- and temperature-controlled room after resting for at least 10 min in the supine position. Participants wore a blood pressure cuff on their right upper arm to measure PWA. The blood pressure cuff automatically inflated to measure the brachial blood pressure and after deflating, it re-inflated to capture PWA waveforms. We conducted PWA at least three times, and the mean of two values which ranged within ±5 mmHg in blood pressure, ±5 beats/min in heart rate, and ±3% in augmentation index (AIx) was used for the further analysis.

#### *2.3. Data Analysis*

Bilateral index (%) of maximal handgrip force output (MF) was calculated by the following equations [35]. The values of bilateral index below zero indicate that bilateral motor performance was less than the sum of unilateral motor performance from each hand, so more negative values of bilateral index denote greater bilateral deficit patterns.

$$\text{Bilateral index} \left( \% \right) = \left( 100 \times \frac{\text{Bilateral hands MF}}{\left( \text{Dominant hand MF} + \text{Non} - \text{dominant hand MF} \right)} \right) - 100$$

Based on the brachial waveforms obtained from the blood pressure cuff, central aortic pressure waveforms were automatically calculated by the mathematical transfer function [36–38]. Central pulse pressure (cPP) is the difference between central systolic blood pressure (cSBP) and central diastolic blood pressure (cDBP). In addition, AIx (%), a measure of arterial stiffness, is calculated as the ratio of augmentation pressure (i.e., cSBP–inflection pressure) and cPP. Increased values of cPP and AIx may be related to a higher appearance rate of cardiovascular disease [39–41].

For statistical analyses, we performed an independent *t*-test to compare the differences of the bilateral index and maximal force production of unilateral hand and both hands between late postmenopausal and young premenopausal women. In addition, one sample *t*-test was used for determining whether the bilateral index for each group was significantly different from zero. For the late postmenopausal women group, Pearson's correlation analyses were performed to determine potential relations of maximal hand-grip forces of unilateral hand and both hands to bilateral deficit index as well as cardiovascular disease risk factors. Using the Shapiro–Wilk test, we confirmed that all dependent variables met the assumption of normality. Statistical analyses were performed using IBM SPSS Statistics version 25 (SPSS Inc, Chicago, IL, USA) with alpha set at 0.05.

#### **3. Results**

#### *3.1. Maximal Hand-Grip Force Production*

Maximal force production in late postmenopausal women was significantly lower than that in young premenopausal women, respectively, in the dominant hand (*t*<sup>38</sup> = −3.26, *p* = 0.002), nondominant hand (*t*<sup>38</sup> = −2.26, *p* = 0.03), and both hands (*t*<sup>38</sup> = −3.63, *p* = 0.001; Figure 2A). Furthermore, the bilateral index values were significantly different between the late postmenopausal and young premenopausal women groups (*t*<sup>38</sup> = −2.68, *p* = 0.011; Figure 2B). One sample *t*-test revealed that the bilateral index values in late postmenopausal women were significantly less than zero (*t*<sup>19</sup> = −2.24, *p* = 0.037), indicating bilateral deficit patterns, whereas the bilateral index values in young premenopausal women were not significantly different from zero (*t*<sup>19</sup> = 1.59, *p* = 0.13). These findings indicate that late postmenopausal women had reduced maximal hand-grip force in unilateral and bilateral tests and bilateral deficit patterns as compared to those in the young premenopausal women group.

**Figure 2.** Maximal force production and bilateral index during isometric hand-grip force production tasks (M ± SE). (**A**) Maximal force production and (**B**) bilateral index. Asterisk (\*) indicates significant difference (*p* < 0.05) between late postmenopausal and young premenopausal women. Number sign (#) indicates significant difference (*p* < 0.05) from zero.

#### *3.2. Correlation Findings for Late Postmenopausal Women*

Late postmenopausal women showed significant correlations between greater bilateral deficit patterns and more reduction of maximal hand-grip forces produced by the dominant hand and both hands, respectively (Table 2). Moreover, increased values of cPP were significantly related to less maximal hand-grip forces produced by the nondominant hand, dominant hand, and both hands, respectively. These findings indicate that decreased maximal hand-grip forces in the dominant hand and both hands were related to more bilateral deficit patterns and difference between cSBP and cDBP in late postmenopausal women.


**Table 2.** Correlation findings in late postmenopausal women.

Note: MF, maximal hand-grip force; asterisk (\*) indicates *p* < 0.05.

#### **4. Discussion**

This study examined bilateral deficit patterns between late postmenopausal and young premenopausal women by estimating the maximal hand-grip force production. Late postmenopausal women showed significantly less hand-grip forces produced in both unilateral (i.e., dominant and nondominant hand) and bilateral tests, and further revealed greater bilateral deficit patterns than young premenopausal women. For late postmenopausal women, decreased maximal hand-grip forces generated by the dominant hand and both hands were significantly related to greater bilateral deficit patterns and increased values in central pulse pressure.

Despite inconsistent findings on the presence of a bilateral deficit pattern in the aging population [28,42], we found that a greater bilateral deficit in the upper extremities appeared in late postmenopausal women. These results expanded previous findings that mainly reported the bilateral deficit phenomenon in the lower extremities [24–28]. Reduced maximal hand-grip forces from each hand during bilateral contraction as compared to those during unilateral contraction may be related to higher interhemispheric inhibition between hemispheres in late menopausal women. Some previous studies asserted that bilateral deficit may be related to suppressive effects of interhemispheric inhibitions between hemispheres during bilateral movement execution [43,44]. In unimanual contraction, increased interhemispheric inhibition from the dominant hemisphere may influence the nondominant hemisphere to suppress the mirror movements of contralateral extremities [45,46]. In a bilateral contraction, both hemispheres may be affected by interhemispheric inhibitions, and these suppressions potentially interfere with motor outputs from each limb [47–49]. Interestingly, previous studies reported that greater levels of interhemispheric inhibition in premenopausal women were related to decreased estradiol level during the ovarian cycle, whereas these changes in interhemispheric inhibition level were not observed in males between pre- and post-tests with an interval of 14 days [50,51]. These findings raised a possibility that greater interhemispheric inhibition levels in late postmenopausal women induced by estrogen deficiency may be related to their bilateral deficit patterns during maximal hand-grip force production.

Moreover, our correlation findings indicated that greater reduction of maximal handgrip strength in the dominant hand was significantly related to increased bilateral deficit patterns in late postmenopausal women. Previous studies reported that maximal handgrip strength of the dominant hand in postmenopausal women significantly decreased as compared to those in either premenopausal women or age-matched men because of potential interactive effects of aging and estrogen deficiency [16,52]. Impaired muscle strength is frequently observed in older adults because of decreased muscle mass and quality (i.e., muscle strength per muscle mass) as referred to age-related sarcopenia [53]. Moreover, the occurrence rate of sarcopenia highly increases around 50s in women who may experience menopause [54,55]. Several studies posited that estrogen may show an anabolic effect on muscles by stimulating insulin-like growth factor-1 (IGF-1) receptors [56], and decreased levels of estrogen may be related to greater oxidative stress that potentially engenders muscle atrophy [57–59]. Moreover, postmenopausal women may have deficits in activation of estrogen receptors highly observed in type II muscle fibers [60,61] influenced by less estrogen and IGF-1 levels, and the deactivation of estrogen receptors presumably impairs muscle strength [58,62]. Consequently, estrogen deficiency in late postmenopausal

women may facilitate functional impairments in the dominant hand related to increased bilateral deficits.

In addition, we found that higher cPP in late postmenopausal women was significantly related to less maximal hand-grip force produced by dominant and nondominant hand and both hands. Given the significant relationship between hand-grip force and muscle mass [63], our correlation findings support a proposition that sarcopenic older women showed higher levels of brachial pulse pressure than nonsarcopenic participants [64]. A potential mechanism underlying the relation of muscle mass to altered pulse pressure involves systemic inflammation markers. Increased circulating inflammation markers (e.g., c-reactive protein, interleukin–6, and tumor necrosis factor-alpha) were associated with reduced muscle strength and mass [65], and more inflammation markers may elevate pulse pressure by inducing endothelial dysfunction, increased arterial stiffness, and decreased nitric oxide bioavailability [66,67]. Higher pulse pressure is often associated with an increase of overall cardiovascular events and mortality of cardiovascular diseases [39,68]. Especially in postmenopausal women, managing risk factors of cardiovascular diseases is important because estrogen deficiency caused by menopause rapidly increases the risk of cardiovascular mortality [69]. Potentially, maximal hand-grip force production in either unilateral or bilateral conditions may additionally indicate risk of cardiovascular events in late postmenopausal women.

Although we found bilateral deficit patterns in late postmenopausal women, some limitations that should be cautiously interpreted remain in this study. First, we did not control the ovarian cycle and measure sex hormones in young premenopausal women. Given that estradiol concentrations are presumably related to levels of interhemispheric inhibition [50,51], different ovarian cycles in young premenopausal women might affect the bilateral index during maximal bilateral hand-grip contraction. Thus, future studies need to measure the bilateral index in young premenopausal women throughout the ovarian cycle to assess potential effect of estradiol levels on bilateral deficit patterns. Second, the current bilateral deficit patterns in late postmenopausal women may be influenced by interactive effects of aging and estrogen deficiency. To determine the potential effects of sex hormones on bilateral deficit patterns, future studies need to specify the relationship between altered levels of sex hormones and bilateral deficits in late postmenopausal women, and further test changes in bilateral deficits after hormone therapy interventions. Third, the lower levels of physical activity levels in late postmenopausal women may influence bilateral deficit patterns in their upper extremities, because older women with high levels of physical activity revealed greater muscle strength that potentially decreased bilateral deficit patterns [70]. Although we did not measure and specify different physical activity levels for late postmenopausal women, the potential relationship between physical activity and bilateral deficits in the upper extremities should be investigated in future studies. Lastly, in this study, we did not report the potential effects of greater bilateral deficits and less grip strength in the dominant hand on the execution of activities of daily living in late postmenopausal women. However, previous studies that focused on lower limb function found the relationship between greater bilateral deficits and more impaired daily living performances (e.g., rising from a chair) [24,25]. Despite no functional assessments on upper extremities for this study, further studies should determine whether bilateral deficit patterns in postmenopausal women are associated with activities of daily living requiring successful bimanual upper limb movements.

#### **5. Conclusions**

In conclusion, this study revealed bilateral deficit patterns in upper extremity for late postmenopausal women. Furthermore, decreased maximal hand-grip force production in the dominant hand was significantly related with greater bilateral deficit patterns for late postmenopausal women. Increased maximal hand-grip force in the dominant and nondominant hands and both hands correlated with decreased central pulse pressure. These findings suggest that age-related impairments in muscle strength and estrogen deficiency in

late postmenopausal women may interfere with conducting successful activities of bilateral movements. Moreover, estimating the dominant hand's maximal force production may provide beneficial information on progressive bilateral deficit patterns and risk factors of cardiovascular disease in late postmenopausal women.

**Author Contributions:** Conceptualization, M.-H.H. and N.K.; methodology, J.-S.K., M.-H.H. and N.K.; software, J.-S.K., M.-H.H. and N.K.; data curation, J.-S.K., M.-H.H. and N.K.; writing—original draft preparation, J.-S.K., M.-H.H. and N.K.; writing—review and editing, J.-S.K., M.-H.H. and N.K.; visualization, J.-S.K., M.-H.H. and N.K.; supervision, N.K.; project administration, N.K.; funding acquisition, N.K. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was funded by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT), grant number NRF-2018R1C1B5084455.

**Institutional Review Board Statement:** The study was conducted according to the guidelines of the Declaration of Helsinki and approved by the Institutional Review Board of Incheon National University (approval# 7007971-201810-002A and the study protocol was approved on 16 December 2020).

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study.

**Data Availability Statement:** Not Available.

**Acknowledgments:** We thank the study participants for their time and effort.

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

#### **References**

