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Article

The Effect of 6-Month Complex Exercise on Serum Bone Metabolism: Focused on the Elderly over 75 Years Old

by
A-Ram Kim
1,
So-Eun Lee
2,
Yoo-Jin Shim
1,* and
Seung-Wook Choi
1,*
1
Department of Sport Leisure, Sungshin Women’s University, Bomun-ro 34da-gil, Seongbuk-gu, Seoul 02844, Korea
2
College of Wesley Creative Convergence, Hyupsung University, Hwaseong-si 18330, Korea
*
Authors to whom correspondence should be addressed.
Appl. Sci. 2022, 12(22), 11373; https://doi.org/10.3390/app122211373
Submission received: 13 October 2022 / Revised: 5 November 2022 / Accepted: 7 November 2022 / Published: 9 November 2022
(This article belongs to the Special Issue Biotechnology and Sports Engineering II)
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Abstract

:
Korea already entered the aging society (August 2017), in which 14% of the population is 65 years or older, and it is expected to enter as a super-aged society, in which 20% of the population is elderly at the world’s fastest rate by 2025. This means that a health management plan is needed to effectively manage the health of the elderly in preparation for the upcoming super-aging society. Therefore, this study analyzed the effects of exercise on serum osteocalcin, bone ALP, and estradiol, which are representative indicators of bone formation after six months of complex exercise, and confirmed the usefulness of exercise programs and biochemical indicators for the elderly in late years to provide basic data for the prevention of osteoporosis. The subjects of this study were the elderly in late years (exercise group = 14, control group = 15), those 75 years or older in Korea, who performed complex exercises twice a week for six months. As a result of analyzing the effect of exercise performance on osteocalcin in the elderly in late years for six months in this study, no significant difference was found. However, osteocalcin decreased by 7.7% in the control group and increased by 18.66% in the exercise group, while ALP increased by 18.92% in the control group and significantly increased by 69.81% in the exercise group. As a result of analyzing the effect on estradiol, there was no significant difference, but it decreased by 55.09% in the control group and decreased by 1.85% in the exercise group. Based on the results showing that exercise clearly plays a positive role in improving bone density even for middle- and late-aged elderly people, in the future, the exercise will be useful to maintain and improve health related to the skeleton of the elderly through the combined participation of aerobic, resistance, and balance exercises. In addition, it is necessary to conduct repeated studies targeting the elderly of various age groups to evaluate the effects of exercise according to period and gender.

1. Introduction

Korea already entered the aging society (August 2017), in which 14% of the population is 65 years or older, and is expected to enter a super-aging society in 2025 at the world’s fastest rate, in which 20% of the population is elderly [1]. Ahead of the super-aged society, now the elderly are intensely interested in health and aging prevention while pursuing healthy life expectancy; not simply living long, but living long healthily. This period is where physical function changes are experienced with increasing age [2]. In Korea, 84.0% of the total elderly were diagnosed with chronic diseases that persist for three months or longer, and those with two or more chronic diseases account for 54.9% of the total elderly [3]. This means that health management measures are needed to effectively manage the health of the elderly in preparation for the upcoming super-aging society [4].
Osteoporosis attracts attention along with high blood pressure, diabetes, hyperlipidemia, arthritis, and back pain, which are representative chronic diseases in Korea. In particular, osteoporotic fractures increase in frequency with age and increase the possibility of morbidity and mortality due to fractures, so the management of bone density is vital for the elderly [5].
It was reported that the risk of fracture is 2.9–7.4 times higher in the hip joint and 3.8–7.4 times higher in the spine for the elderly with osteoporosis compared to those who have no osteoporosis [6]. It is known that these risk factors for osteoporosis include demographic factors such as age, race, gender, and menopause, medical factors such as diseases and drugs, and lifestyle factors such as nutritional deficiencies and sedentary lifestyle [7], and a recent study reported that it is closely related to the appropriate body circumference in old age [8]. On the other hand, it is reported that every 0.44 falls in osteoporotic female patients increases the risk of hip fracture by 1.5 times, and the risk of death within 2 years is reported to increase by about 2.1 times [9,10].
In fact, according to NHANES in the United States, about 50% of women and 12% of men over 85 years old had osteoporosis prevalence [11], and 93% of women over 80 years of age used to have at least one fracture. In Korea, the number of fracture patients by age group over the past five years was 37.4% in their 80s (annual average 8.3%) in 2020, 26.3% in their 60s (annual average 6.0%), and 14.1% (annual average 3.4%) in their 70s compared to 2016. The number of patients treated for fractures was more for women than men from the age of 50 or older [12]. Additionally, in the UK, NHS pays GBP 4.4 billion annually for fragility fractures [13]. In the United States, it is estimated that they paid USD 57 billion for osteoporosis in 2018, and this shows that more than 95 billion US dollars per year will be required till 2040 [14]. An effective osteoporosis prevention strategy is essential in view of the increase in life expectancy worldwide and the burden that osteoporosis-induced fractures put on society, medical systems, and individuals.
For the prevention and treatment of osteoporosis, it is a general guideline to recommend quitting smoking, calcium intake, and exercise in addition to drugs. In particular, studies showing that taking a bed rest that does not support body weight may cause loss of bone density, and significant changes in bone composition relatively explains the need for exercise [15]. Therefore, many studies for activities using a single body part [16], such as exercise [17,18,19,20,21], walking [22,23], or sports [24] focusing on specific types of physical activity, were carried out with middle-aged women, adolescents, and men. However, despite the transitional period of functional loss [25], studies focusing on the elderly in the late years are not sufficient. There are still many different opinions on the effect of exercise on improving performance the bone density of the elderly.
Starting from the age of 75, due to a decrease in daily living ability and physical strength, depending on others, or needing to use an orthosis or cane, the service must be provided in a different way according to the characteristics of the age [26], but most of the studies for exercise programs [27,28,29,30] were conducted for all age groups without any age classification.
In the case of response to osteoporosis treatment, a long-term study is necessary because bone density tests appear 1 to 2 years later, and bone remodeling does not work well due to aging [31]. In the case of biochemical bone markers, there is an advantage in that the treatment effect can be checked within a short period of time by showing a change of 30 to 70% within 3 to 6 months [32].
Therefore, this study analyzed the effects of exercise on serum osteocalcin (OC), bone ALP [33], and estradiol, which are representative indicators of bone formation after six months of complex exercise, and analyzed the exercise program and biochemical indicators. This study aims to provide basic data for the prevention of osteoporosis of the elderly by confirming the usefulness of the exercise program and biochemical markers.

2. Methods

2.1. Subjects of the Research

The subjects of this study were women, who were randomly selected and assigned to the elderly aged 75 years or older (exercise group = 14, control group = 15) who used one public health center located in S city, South Korea. Prior to the study, an orientation was held to explain the test and exercise, and the subjects understood the purpose and method of the study, and had no problems with verbal communication and decision making, and had no physical defects or diseases. In addition, those who took drugs, smoked, drank alcohol, etc., for a long time were excluded from the subjects. This experimental protocol was approved by the Institutional Review Committee of Sungshin Women’s University (SSWUIRB-2021-015) and was conducted with prior consent of all participants. Thirty-six elderly women were selected, but seven women who failed to participate in the study till the end were excluded. The characteristics of the participants are as follows <Table 1>.

2.2. Measuring Items and Methods

2.2.1. Physical Examination

In the case of height, using a digital extensometer (NeoGMTEC Co., Ltd., Seoul, Korea), the subject was asked to keep the eyes in a horizontal position and chin in the upright position, and then the vertical distance from the sole to the two vertices was measured (measurement values were recorded in units of 0.1 cm). In addition, in the case of bodyweight, after undressing, it was placed in the center of the scale and recorded to one decimal place, and the unit was recorded in kg.

2.2.2. Blood Analysis

To measure osteocalcin, bone ALP and estradiol (E2), 5 mL of blood was collected from the antecubital vein using a disposable syringe between 8 and 9 am on the same day under fasting for 2 h. After clotting at room temperature for more than 30 min, centrifugation was performed at 3000 rpm (or 3500× g) for 5 to 10 min, and the supernatant was transferred to an EP tube and then measured.

2.2.3. Exercise Program

The complex exercise was performed twice a week for six months. For exercise intensity, the exercise duration was gradually adjusted to an exercise intensity of 45–55% of HRRmax, considering that the study subject were elderly women over 75 years old, using Karvonen’s formula. Resistance exercise was performed at 11–14 RM, for three sets. In the case of balance exercise, a single leg standing exercise for 1 to 2 min, rest for 30 s, and other various movements (including movements such as single leg standing with another leg lifting forward, lifting aside, lifting back, and bening), was performed for the duration of the single leg standing and the frequency was gradually increased. The exercise was conducted in a public health center, and one professional instructor guided then exercise for 6 months. The exercise consisted of a 5 min warm-up exercise, 5 min cool-down exercise, and the main exercise. The main exercise was a complex exercise and consisted of 20 min of aerobic exercise, 20 min of resistance exercise, and 10 min of balance exercise. The exercise program is as follows <Table 2>.

2.2.4. Data Processing

All data measured in this study were expressed as descriptive statistics (mean, standard error of the mean: SE) using the upper statistical program of SPSS PC + for window (version 22.0), and the detailed processing method is as follows:
Mean (M) and standard deviation (SD) were calculated for all variables, one-way ANOVA was performed to check the interaction between groups and measurement time, and a t-test was performed before and after the group’s analysis. The significance level was set as α = 0.05.

2.3. Data Procesing

(1) Shapiro–Wilk was conducted for a preliminary normality test for the exercise group and the control group. After carrying out the normality test, a statistical method was applied according to the nonparametric analysis (Wilcoxon, Mann–Whitney) and the parametric analysis (paired t-test and independent t-test).
(2) In order to verify the difference in changes observed in the dependent variables within each group with normality, a paired t-test was performed. In addition, in order to examine the difference in variables by the measurement period between the groups, an independent t-test was conducted.
(3) Wilcoxon was carried out in order to verify the difference in changes in dependent variables within each group without normality, while Mann–Whitney was conducted in order to inquire into the difference in variables by the measurement period between the groups.
(4) The two-way repeated measures ANOVA was performed to make a simultaneous analysis of the differences in the mean of dependent variables between two groups (exercise group and control group) and between two tests (pre-test and post-test).
(5) The significance level of all statistical analyses was set to <0.05.

3. Result

The mean and standard deviation of osteocalcin, bone ALP, and estradiol in each group can be summarized as follows <Table 3>.

3.1. Results of Osteocalcin

The 6-month complex exercise analysis results are shown in Table 2 and Figure 1. In the case of osteocalcin, the control group was 9.18 ± 3.09 ng/mL before exercise and 8.47 ± 3.54 ng/mL after exercise, and the exercise group was 8.04 ± 3.93 ng/mL before exercise and 9.54 ± 5.48 ng/mL after exercise, showing no significant difference in both groups.
As a result of analyzing the interaction effect according to the group, the F statistic value was 0.001, the F statistic value according to the measurement period was 0.132, and the F statistic value for the interaction between the group and the measurement period was 1.057, which was not significant at all <Table 4, Figure 1>.

3.2. Results of ALP

The result of the 6-month complex exercise analysis is shown in Table 2 and Figure 1. In the case of ALP, there was no significant difference in the control group at 10.15 ± 3.91 ug/L before exercise and 12.07 ± 3.71 ug/L after exercise, but in the exercise group, it was 7.75 ± 4.47 ug/L before exercise and 13.16 ± 4.43 ug/L after exercise, showing a significant difference.
As a result of analyzing the interaction effect according to the group, the F statistic value was not significant at 0.365, and the F statistic value was 11.359, indicating a significant difference as a result of testing whether it affects ALP according to the measurement period <Table 5, Figure 2>.

3.3. Results of Estradiol

The result of the 6-month complex exercise analysis is shown in Table 2 and Figure 1. For estradiol, the control group was 11.29 ± 12.17 pg/mL before exercise and 5.07 ± 0.25 pg/mL after exercise, and the exercise group was 14.09 ± 12.76 pg/mL before exercise and 13.83 ± 13.77 pg/mL after exercise, which showed no significant difference between both groups.
As a result of analyzing the interaction effect according to the group, the F statistic value was 0.001, the F statistic value according to the measurement period was 0.132, and the F statistic value for the interaction between the group and the measurement period was 1.057, which did not show a significant difference <Table 6, Figure 3>.

4. Discussion

This study analyzed the effects of an exercise program on the representative serum osteocalcin, bone ALP, and estradiol as indicators of bone formation after 6 months of complex exercise for elderly women aged 75 years or older using public health centers in order to provide a basis for its use.
This study analyzed the effect of exercise performance on osteocalcin for six months in the elderly in late years. Although there was no significant difference, osteocalcin in the control group decreased by 7.7%, and osteocalcin in the exercise group increased by 18.66%. Osteocalcin differs depending on aerobic exercise and resistance exercise [34]. As a result of 16 weeks of resistance exercise in postmenopausal women, it was reported that there was no change in osteocalcin, an indicator of bone formation [35], and there was also a report [36] that postmenopausal women’s exercise treatment did not change with osteocalcin. Additionally, exercise performance in postmenopausal women increases bone mineral density, but does not change serum osteocalcin levels [37]. However, according to Smith et al. [38], osteocalcin increased when anaerobic exercise was performed for 1 to 2 months [39], and low-intensity and high-intensity ladders for 6 weeks in mature male rats. As a result of exercise, the serum osteocalcin concentration was significantly increased in both groups compared to the control group, but bone density was significantly increased only in the high-intensity exercise group. Therefore, it is judged that exercise performance plays a positive role in improving maximum bone mass and bone density [40].
It was reported that ALP is a representative index reflecting the activity of osteoblasts [41] and can be used as an index of bone metabolism in subjects without liver disease or metabolic disease.
As a result of analyzing the effect of exercise performance on ALP for six months in the elderly in late years in this study, the control group increased by 18.92%, and the exercise group significantly increased by 69.81%. This study, together with Rudberg et al. [42], which reported that bone-type alkaline phosphatase increased dramatically as a result of performing a bicycle ergometer with an average age of 57 years old, a report which claimed that the concentration of BALP was high [43], a report which claimed that the bone BALP increased after 12 weeks compared to pre-exercise only in the aqua aerobic exercise group [13], and the report of Swissa-Sivan et al. [44], which claimed that growing rats after swimming exercise for 12 weeks showed bone density higher by 13%, and bone content higher by 10% and 67% higher ALP than the control group, respectively, proved that the exercise is effective for the bone density increase in the elderly in late years.
However, serum osteocalcin and ALP were increased at the time of menopause due to the compensatory process by the osteogenesis inhibitory action [45,46,47] and osteoporosis. The analysis results on the pattern of the bone formation index change according to exercise treatment in postmenopausal women with prognoses are still not clear. Therefore, along with a number of reports [48,49], which claim that the effect on bone metabolism is different depending on the type of exercise, it is also affected by the duration of exercise [47]. To use it as an analysis index of metabolism, further analysis is required, including many cases in the future.
Among endocrine hormones, aging-related hormones include growth hormone, DHEA-S (dehydroepiandrosterone sulfate), and estrogen, and these hormones show a decrease in secretion with aging [49]. After menopause, estradiol (E2), which accounts for most estrogen, is not produced, and trace levels of E2 appear [50]. This study analyzed the effect of complex exercise performance on estradiol for 6 months in the elderly in late years. Although no significant difference was found, the control group decreased by 55.09%, and the exercise group decreased by 1.85%.
Lanfrancok et al. [51] found that estrogen increased significantly in both male and female elderly in a study conducted with resistance exercise for the elderly, whereas [52] showed that estradiol decreased after completing 12 weeks of a complex exercise program. In addition, with the application of a 12-week circular exercise program [53], an elastic resistance exercise program using a rip trainer [54], and an aerobic exercise program [55], it is reported that there is a positive improvement effect by increasing E2.
Therefore, it was found that although women hardly produce E2 as they age and enter menopause, regular physical activity can synthesize trace amounts of E2 [54].
In this study, estradiol decreased in both groups, but the exercise group showed a slight decrease compared to the control group, so exercise is judged to be able to delay the decrease in estradiol levels due to aging.
Bone is sensitive to external mechanical stimuli, as well as to metabolic changes in the body to cause changes in activity. Changes in bone metabolism that cause increases and decreases in bone mass include genetic factors [56], as well as environmental factors, such as nutrition [57] and exercise [58], causing a significant impact on inactivity environments, such as space flight [59] or weightlessness [60], promoting bone mass loss. However, regular moderate exercise maintains or increases bone mass and is known to cause the disease [20]. Physical activity and exercise play a role in preserving bone density by increasing osteoblast activity [61], and Nuti et al. [62] also found that exercise patterns differed in growth, adolescence, and old age. However, there was an increase in bone density due to exercise. In addition, many studies show that exercise is associated with bone formation [63,64,65,66] and it is reported that the exercise has a significant effect on improving bone mineral density [67].
Looking at the above results in general, it is necessary to maintain and promote physical activity for health management of the elderly, and strategies to increase the current low rate of physical activity are required. Therefore, it is necessary to understand the physical characteristics and physical activity of the elderly. Since this study was limited to the female elderly, it is necessary to secure subjects of various age groups, including male elderly, in the future study. The rate of aging varies from person to person [68], and the physical response and adaptation to physical activity may vary according to age [69], and diseases of the elderly also vary according to age. For this reason, the exercise program should be conducted differently by dividing the elderly by age.

5. Conclusions

This study is an experimental study, which attempted to check the effect of an exercise program on osteocalcin, ALP, and estradiol in middle and late-stage elderly (over 75 years old), and was effective in maintaining and improving osteocalcin, ALP, and estradiol.
It will be important to improve bone metabolism-related health and other health through continuous participation in exercise by developing and providing an exercise program for the elderly based on the results that exercise clearly plays a positive role in improving bone mineral density even for middle- and late-stage elderly people.
Such efforts can be an alternative that can efficiently cope with various problems caused by the increase in the elderly population at a low cost. In the future, it will be necessary to conduct a long-term program of at least 6 months or longer and carry out repeated studies on elderly people of various age groups to evaluate the effects of exercise according to period and gender.

Author Contributions

Conceptualization, A.-R.K.; Data curation, S.-E.L.; Formal analysis, A.-R.K.; Investigation, S.-E.L.; Resources, Y.-J.S.; Software, Y.-J.S.; Supervision, S.-W.C.; Writing—original draft, A.-R.K.; Writing—review & editing, S.-W.C. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Ministry of Education of the Republic of Korea and the National Research Foundation of Korea (NRF-2020S1A5B5A17089936).

Institutional Review Board Statement

This experimental protocol was approved by the Institutional Review Committee of Sungshin Women’s University (SSWUIRB-2021-015) and informed to and received the consent of all participants.

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Conflicts of Interest

The authors declare no conflict of interest.

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Applsci 12 11373 g001 550
Figure 1. Osteocalcin changes.
Figure 1. Osteocalcin changes.
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Applsci 12 11373 g002 550
Figure 2. ALP changes (** p < 0.01).
Figure 2. ALP changes (** p < 0.01).
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Applsci 12 11373 g003 550
Figure 3. Estradiol changes.
Figure 3. Estradiol changes.
Applsci 12 11373 g003
Table
Table 1. Characteristics of the study participants.
Table 1. Characteristics of the study participants.
VariableControl Group
(Mean ± SE)		Exercise Group
(Mean ± SE)		p-Value
Age (year)80.80 ± 2.3781.14 ± 3.980.429
Height (cm)154.59 ± 2.14155.14 ± 3.050.992
Weight (kg)57.68 ± 3.1559.26 ± 4.140.791
Table
Table 2. The 6-month complex exercise program for the elderly aged over 75 years.
Table 2. The 6-month complex exercise program for the elderly aged over 75 years.
VariableTypeTimeFrequencyIntensity
Warm-up exerciseStretching5 minTwice a weekRPE 2~3
Main exerciseAerobic exerciseWalking in place
7 m shuttle walking		20 minHRmax
45~55%

11~14 RM
3 set
Resistance exerciseBiceps curl, triceps curl, side band squat, kick back, knee up20 min
Balance exerciseOne-leg standing10 min
Cool-down exerciseStretching5 minRPE 2~3
Table
Table 3. Changes in osteocalcin after 6-month compound exercise.
Table 3. Changes in osteocalcin after 6-month compound exercise.
VariablePrePostp
Osteocalcin
(ng/mL)		control group9.18 ± 3.098.47 ± 3.540.603
exercise group8.04 ± 3.939.54 ± 5.480.683
ALP
(ug/L)		control group10.15 ± 3.9112.07 ± 3.710.181
exercise group7.75 ± 4.4713.16 ± 4.430.003
Estradiol
(pg/mL)		control group11.29 ± 12.175.07 ± 0.250.946
exercise group14.09 ± 12.7613.83 ± 13.770.325
Table
Table 4. Results of two-way ANOVA analysis of osteocalcin.
Table 4. Results of two-way ANOVA analysis of osteocalcin.
VariableSSdfMSFp Valuep eta-sq
Corrected model19.43336.4790.3890.7620.021
Intercept4492.61514492.615269.5200.0000.833
Group0.01710.0170.0010.978
Time2.20012.2000.1320.718
Group × Time17.623117.6231.0570.308
Error900.1245416.669
Total5418.12058
Corrected total919.55757
Table
Table 5. Results of two-way ANOVA analysis of ALP.
Table 5. Results of two-way ANOVA analysis of ALP.
VariableSSdfMSFp Valuep eta-sq
Corrected model238.357379.4524.6510.0060.205
Intercept6734.30316734.303394.2290.0000.880
Group6.24116.2410.3650.5480.007
Time194.0301194.03011.3590.0010.174
Group × Time44.197144.1972.5870.1140.046
Error922.4405417.082
Total7917.28058
Corrected total1160.79757
Table
Table 6. Results of two-way ANOVA analysis of estradiol.
Table 6. Results of two-way ANOVA analysis of estradiol.
VariableSSdfMSFp Valuep eta-sq
Corrected model775.1763258.3922.0960.1110.104
Intercept7097.47317097.47357.5800.0000.516
Group484.5241484.5243.9310.0530.068
Time152.2351152.2351.2350.2710.022
Group × Time128.4281128.4281.0420.3120.019
Error6656.24954123.264
Total14409.88058
Corrected total7431.42457
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Kim, A.-R.; Lee, S.-E.; Shim, Y.-J.; Choi, S.-W. The Effect of 6-Month Complex Exercise on Serum Bone Metabolism: Focused on the Elderly over 75 Years Old. Appl. Sci. 2022, 12, 11373. https://doi.org/10.3390/app122211373

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Kim A-R, Lee S-E, Shim Y-J, Choi S-W. The Effect of 6-Month Complex Exercise on Serum Bone Metabolism: Focused on the Elderly over 75 Years Old. Applied Sciences. 2022; 12(22):11373. https://doi.org/10.3390/app122211373

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Kim, A-Ram, So-Eun Lee, Yoo-Jin Shim, and Seung-Wook Choi. 2022. "The Effect of 6-Month Complex Exercise on Serum Bone Metabolism: Focused on the Elderly over 75 Years Old" Applied Sciences 12, no. 22: 11373. https://doi.org/10.3390/app122211373

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