Regular aerobic exercise improves sexual function assessed by the Aging Males’ Symptoms questionnaire in adult men

Abstract

The leading cause of aging-induced male-specific disorders such as physical, mental and/or sexual symptoms is testosterone deficiency. Although aerobic exercise is suggested to improves circulating testosterone levels, physical fitness, depressive symptoms, and sexual function, the effect of regular aerobic exercise on aging-induced disorders has not yet been clarified. Here we performed cross-sectional and interventional studies to identify the effect of aerobic exercise on aging-induced disorders assessed by the Aging Males’ Symptoms questionnaire (AMS). In study 1, the relationship between aerobic exercise capacity (i.e. peak oxygen consumption) and AMS scores were cross-sectionally examined in 169 adult men. In study 2, the effect of a 12-week regular aerobic exercise on AMS scores was longitudinally investigated in 18 adult men. In study 1, the AMS-total, AMS-somatic, AMS-psychological, and AMS-sexual scores were significantly correlated to aerobic exercise capacity even after considering age and testosterone levels. In study 2, 12-week aerobic exercise training significantly improved AMS-sexual and tended to improve AMS-total scores. Additionally, an increase in vigorous physical activity was correlated to improve in the AMS-sexual score. These results suggest that regular aerobic exercise is an effective strategy to improve aging-induced disorders in men.

Keywords:

• Physical fitness
• peak oxygen consumption
• aerobic exercise
• testosterone
• male sexual function

Introduction

An aging-induced decrease in circulating testosterone levels adversely influences several functions such as physical, psychological, and/or sexual functions [1–5] and lowers the quality of life in men [6]. In clinical situations, the typical treatment for these disorders is testosterone replacement therapy, and it shows positive effects on physical fitness, mood, and sexual function [7–11]. However, testosterone replacement therapy also has the potential risk for side effects in men [12]. Therefore, it is preferable to establish an alternative treatment or a method that maximizes the effect of testosterone supplementation on aging-induced disorders in men.

Previous studies have suggested that regular aerobic exercise improved circulating testosterone levels in healthy young, old, or overweight/obese men [13–18]. Besides, aerobic exercise is also associated with improvements in sexual function [19,20], depressive symptoms [21], and physical fitness [22,23]. Hence, improved aerobic fitness may be effective for not only circulating testosterone levels but also aging-induced disorders in men. However, these possible associations among aerobic fitness and aging-induced disorders in men have not been fully clarified yet.

Here we hypothesized that aerobic exercise is protective against aging-induced disorders in men. To confirm our hypothesis, we performed cross-sectional and interventional studies to identify the effect of aerobic exercise on aging-induced disorders in men.

Materials and methods

Study design and participants

Study 1: cross sectional study

Participants were recruited through local newspaper advertisements and personal contacts. The inclusion criteria were as follows: (1) men; (2) age ≥20 years. The exclusion criteria for the present study were as follows: (1) under 35 years old; (2) presence or history of cardio/cerebrovascular disease (e.g. angina, myocardial infarction, and stroke) assessed using a medical history questionnaire; (3) currently receiving medications for erectile dysfunction (ED) or depression; (4) current smokers. In addition, participants who took meals and/or medications on the morning of the measurement were excluded. A total of 168 adult men were included in the analyses; median [interquartile range] of age was 62 [53–69] years old. The number of participants who were regularly using antihypertensive medication, antidyslipidemic medication, and hypoglycemic medication were 20 (11.8%), 14 (8.3%), and 7 (4.1%), respectively. This study was approved by the ethical committee of the Faculty of Health and Sport Sciences at the University of Tsukuba. The study conformed to the principles outlined in the Helsinki Declaration, and all participants provided written informed consent before inclusion in the study.

Study 2: regular aerobic exercise

Participants were recruited through local newspaper advertisements. The inclusion criteria were as follows: (1) men; (2) age 30–64 years. The exclusion criteria for the present study were as follows: (1) under 35 years old; (2) presence or history of cardio/cerebrovascular disease (e.g. angina, myocardial infarction, and stroke) assessed via a medical history questionnaire. Initially, 24 men were enrolled in this study, but three were excluded under 35 years old and other three were excluded due to a lack of post-training data (n = 1, relocated; n = 1, time; and n = 1, personal issues). A total of 18 adult men were included in the analyses; median [interquartile range] of age was 54 [45–56] years old. This study was reviewed and approved by the institutional review board of the University of Tsukuba. All study procedures and potential risks were explained to the participants and they provided written informed consent to participate in the study. This study 2 was a pre-specified sub-study (secondary analysis) of UMIN000027711 [24].

Subjects participated in an aerobic exercise class for up to 90 min/day, 3 times/week for 12 weeks as previously described [13,22,25–27]. The exercise program included a 15–20 min warm-up session followed by an approximately 40–60 min walking and/or light jogging session, and concluded with a 15–25 min cool-down session. Daily steps and physical activity time in both the aerobic exercise sessions and free-living conditions were assessed using a tri-axial accelerometer (ActiveStyle Pro HJA-750IT; Omuron Healthcare Co. Ltd., Kyoto, Japan). Participants were asked to wear the accelerometer on a belt over their hip both for 2 weeks prior to the aerobic exercise intervention (before intervention) and in the last 2 weeks of the aerobic exercise intervention period (after intervention) and to wear the device at all times while they were awake except when swimming or bathing. For data reduction, a valid day was defined as 10 or more h/day of monitor wear. The PA time was classified as follows: light-intensity physical activity (LPA), 1.6–2.9 metabolic equivalents (METs); moderate-intensity physical activity (MPA), 3.0–5.9 METs; vigorous-intensity physical activity (VPA), ≥6.0 METs; and moderate to vigorous-intensity physical activity (MVPA).

Aging Males’ Symptoms questionnaire (AMS)

The AMS is a self-answer type questionnaire and which assesses aging-induced male specific disorders. The AMS is consists of 17 items, including five psychological symptoms score items (questions 6–8, 11 and 13), seven somatic symptoms score items (questions 1–5, 9 and 10), and five sexual symptoms score items (questions 12 and 14–17) [28,29]. Each item is evaluated with five phases, from 1 point (no symptoms) to 5 points (very severe symptoms) and the range of total scores is 17–85. Severity is classified into four groups based on the range of scores: 17–26 points as no/low symptoms, 27–36 points as mild symptoms, 37–49 points as moderate symptoms, and 50–85 points as severe symptoms.

Aerobic exercise capacity

To measure aerobic exercise capacity as an index of exercise endurance, the subjects performed peak oxygen consumption. To evaluate their aerobic exercise capacity, the subjects performed an incremental cycling ergometer exercise consisting of 2 min at 20 W followed by a 10–20 W increase every one minutes. Aerobic exercise capacity was measured using an online computer-assisted circuit spirometry (AE300S; Minato Medical Science, Osaka, Japan) and peak oxygen consumption was assumed when at least two of the following criteria were satisfied: (1) the participant reaching their age-predicted maximal HR (i.e. 220 − age), (2) Borg scale >19, (3) respiratory equivalent >1.2, or (4) the participant being unable to maintain a pedaling speed <55 rpm [20].

Anthropometric measurements

Body weight was measured to the nearest 0.1 kg using a digital scale. Height was measured to the nearest 0.1 cm using a wall-mounted stadiometer. Body mass index (BMI) was calculated as the participants’ weight (kg) divided by their height (m²). Waist circumference was directly measured on the skin at the level of the umbilicus with the participant in a standing position; measurements were made in duplicate to the nearest 0.1 cm. Visceral fat area was measured using the dual-impedance analysis method (HSD-2000; Omron Healthcare, Kyoto, Japan).

Blood biochemistry

Blood samples were taken in the morning after 12-h overnight fast. Serum concentrations of triglyceride, total cholesterol, high-density lipoprotein (HDL) cholesterol, low-density lipoprotein (LDL) cholesterol, and plasma concentration of glucose and HbA1c were determined using standard enzymatic techniques. Serum total testosterone levels were measured using chemiluminescent immunoassay by commercial laboratory (LSI medience. Ibaraki, Japan).

Statistical analysis

The Shapiro–Wilk test was used to assess the normality of all parameters. Data are expressed as the means ± standard deviation (SD) or frequency counts (for categorical data). Unpaired Student’s t-test and Wilcoxon rank sum test were used to assess the group differences between all parameters. Paired Student’s t-test and Wilcoxon signed rank test were used to assess the group differences between data before and after the 12-week regular aerobic exercise. The relationships among each parameter were analyzed using Spearman’s (r_s) correlation coefficient. Independent correlates of AMS scores were examined by using a multivariate linear regression analysis (independent variables: age, aerobic exercise capacity and testosterone levels). Statistical significance was set a priori at p < 0.05 for all comparisons. Statistical analyses were performed using JMP Pro version 12 (SAS Institute).

Results

Study 1

The characteristics of the studied subjects are summarized in Table 1. Medians of BMI (22.5 kg/m²), waist circumference (82.0 cm), HDL cholesterol (62 mg/dl), LDL cholesterol (125 mg/dl), triglycerides (92 mg/dl), glucose (101 mg/dl), and testosterone (19.8 nmol/l) were within the normal range.

Table 1. Characteristics of studied men (n = 169).

Variable	n = 169
Age, years	60 ± 12
Height, cm	167.3 ± 6.7
Body mass, kg	64.6 ± 10.1
BMI, kg/m^2	23.0 ± 3.1
Waist circumference, cm	82.9 ± 9.9
Visceral fat area, cm^2	64.1 ± 31.0
HDL cholesterol, mg/dl	65 ± 16
LDL cholesterol, mg/dl	126 ± 32
Triglycerides, mg/dl	101 ± 43
Glucose, mg/dl	104 ± 20
HbA1c, mg/dl	5.6 ± 0.6
Testosterone, nmol/l	20.3 ± 6.5
Aerobic exercise capacity, ml/min/kg	26.7 ± 7.4
AMS-total score, points	29 ± 8
AMS-somatic score, points	11 ± 3
AMS-psychological score, points	7 ± 2
AMS-sexual score, points	11 ± 4

Data are shown as the median [interquartile range].

BMI: body mass index; HDL: high-density lipoprotein; LDL: low-density lipoprotein; AMS: Aging Males’ Symptoms.

Aerobic exercise capacity was assessed by peak oxygen consumption.

Table 2 shows the correlations between each variable. Age was significantly correlated with the scores of AMS-total (r_s = 0.152, p < 0.05), AMS-psychological (r_s = −0.197, p < 0.05), and AMS-sexual (r_s = 0.396, p < 0.01) (Table 2). Aerobic exercise capacity was significantly correlated with the scores of AMS-total (r_s = −0.287, p < 0.01), AMS-somatic (r_s = −0.227, p < 0.01), and AMS-sexual (r_s = −0.309, p < 0.01) (Figure 1). On the other hand, serum testosterone levels were not significantly correlated with AMS scores (Table 2). After considering age and circulating testosterone levels, aerobic exercise capacity was significantly associated with AMS-total (β = −0.347, p < 0.01), AMS-somatic (β = −0.370, p < 0.01), AMS-psychological (β = −0.225, p < 0.05) and AMS-sexual (β = −0.223, p < 0.01).

Figure 1. Correlations between aerobic exercise capacity and AMS-total (A), -somatic (B), -psychological (C), and -sexual (D) scores.

Table 2. Relationships between each variable.

	AMS-total	AMS-som	AMS-psy	AMS-sex
Age, years	0.152*	−0.049	−0.197*	0.396**
Height, cm	−0.194*	−0.084	−0.012	−0.252**
BMI, kg/m^2	−0.032	0.073	−0.068	−0.070
Visceral fat area, cm^2	0.010	0.100	−0.088	0.041
HDL cholesterol, mg/dl	−0.069	−0.075	0.099	−0.111
LDL cholesterol, mg/dl	−0.165*	−0.114	−0.021	−0.198*
Triglycerides, mg/dl	−0.053	−0.026	−0.010	0.070
Glucose, mg/dl	0.038	−0.006	−0.075	0.106
HbA1c, mg/dl	0.072	0.022	0.074	0.155*
Testosterone, nmol/l	0.067	−0.011	0.091	−0.066

BMI: body mass index; HDL: high-density lipoprotein; LDL: low-density lipoprotein; VO_2peak: peak oxygen consumption; AMS-total: aging male symptoms-total; AMS-som: aging male symptoms-somatic; AMS-psy: aging male symptoms-psychological; AMS-sex: aging male symptoms-sexual.

**p < 0.01; *p < 0.05.

Study 2

Table 3 shows the characteristics of subjects before and after the 12-week aerobic exercise intervention. Body mass, BMI, waist circumference, and visceral fat area significantly decreased, and physical activity levels and aerobic exercise capacity significantly increased after the aerobic exercise intervention. On the other hand, aerobic exercise training tended to increase serum testosterone levels. Figure 2 shows the AMS scores before and after the intervention. The 12-week regular aerobic exercise significantly decreased the AMS-sexual score and tended to reduce the AMS-total score, but not the AMS-somatic and AMS-psychological scores (Figure 2). Although, the percentage change in serum testosterone levels did not correlate to AMS scores, the percentage change in VPA significantly correlated to that in AMS-sexual score (r_s = −0.539, p < 0.05).

Figure 2. The changes in AMS-total (A), AMS-somatic (B), AMS-psychological (C) and AMS-sexual (D) scores before and after the 12-week regular aerobic exercise.

Table 3. Characteristics of subjects before and after the aerobic exercise intervention.

n = 18	Before	After	p-Value
Age, years	51 ± 8	−	−
Height, cm	170.6 ± 7.0	−	−
Body mass, kg	80.0 ± 8.6	78.0 ± 9.1	<0.001
BMI, kg/m^2	27.5 ± 2.3	26.8 ± 2.4	<0.001
Waist circumference, cm	95.7 ± 6.8	92.5 ± 6.7	<0.001
Visceral fat area, cm^2	93.3 ± 30.5	84.3 ± 26.7	0.004
HDL cholesterol, mg/dl	55 ± 8	56 ± 10	0.326
LDL cholesterol, mg/dl	128 ± 32	128 ± 31	0.998
Triglycerides, mg/dl	126 ± 95	100 ± 45	0.149
Glucose, mg/dl	105 ± 16	101 ± 9	0.142
Testosterone, nmol/l	15.6 ± 5.3	17.2 ± 5.5	0.092
Steps, step/day	8710 ± 4674	10551 ± 3286	0.011
LPA, min/day	315 ± 85	288 ± 83	0.048
MPA, min/day	57 ± 24	64 ± 26	0.079
VPA, min/day	6 ± 23	16 ± 14	0.006
MVPA, min/day	63 ± 45	80 ± 37	0.001
Aerobic exercise capacity, ml/min/kg	26.2 ± 4.1	30.2 ± 4.4	<0.001

BMI: body mass index; HDL: high-density lipoprotein; LDL: low-density lipoprotein; LPA: light physical activity; MPA: moderate physical activity; VPA: vigorous physical activity; MVPA: moderate to vigorous physical activity.

Aerobic exercise capacity was assessed by peak oxygen consumption.

Date are expressed as mean ± SD.

Discussion

In the present study, we investigated the association between aerobic fitness and AMS scores in adult men, and the effect of regular aerobic exercise on the AMS scores in adult men. In the cross-sectional study, aerobic fitness was significantly associated with AMS scores in 169 adult men after considering age and testosterone levels. Furthermore, in the interventional study, the 12-week regular aerobic exercise significantly decreased the AMS-sexual score and tended to decrease the AMS-total score. These results suggest that regular aerobic exercise is an effective strategy to improve AMS scores, especially sexual function in adult men.

The AMS questionnaire is used for the assessment of aging-induced disorders such as somatic, psychological, and sexual functions in men. Several studies have suggested that aerobic exercise associated with sexual function [19,20], depressive symptoms [21], and physical fitness [22,23], implying aerobic exercise effective for AMS scores. Thus, the present study hypothesized that regular aerobic exercise was associated with AMS scores. In the cross-sectional study, high aerobic exercise capacity was associated with low scores of the AMS-total, AMS-somatic, AMS-psychological, and AMS-sexual after considering age and serum testosterone levels in adult men. Additionally, the 12-week regular aerobic exercise significantly decreased the AMS-sexual score and tended to reduce the AMS-total score in the interventional study. Although there were no significant reductions in the AMS-somatic and AMS-psychological scores, the average values of these decreased after the 12-week intervention. It is possible that the duration of the exercise intervention was not enough to improve AMS-somatic and AMS-psychological scores. Taken together, regular aerobic exercise is effective to improve in aging-induced disorders, especially AMS-sexual and AMS-total scores. These findings propose a new option (i.e. regular exercise) for prevention and treatment for aging-induced disorders in men.

In clinical situations, testosterone replacement therapy is a typical treatment strategy for aging-induced disorders such as physical, psychological, and/or sexual functions in men [7–11]. However, testosterone replacement therapy also has the potential risk of negative effects on health [12]. Therefore, it is necessary to establish a way to maximize the effect of modest testosterone supplementation in men. Several studies have demonstrated that a combination of testosterone replacement therapy and exercise had significant improvements in circulating testosterone levels, total AMS score, the International Index of Erectile Function score, and body compositions compared to testosterone replacement therapy alone [30–32]. These previous studies suggested the importance of exercise for the treatment of aging-induced disorders in terms of the combination of testosterone replacement therapy and exercise.

Aging-induced male-specific disorders are suggested to be caused by a decrease in circulating testosterone levels that occurs with aging [1–5]. However, in the present cross-sectional study, no significant associations were found between serum total testosterone levels and AMS scores in men with normal testosterone levels. Besides, changes in serum total testosterone levels did not correlate to AMS scores in the present interventional study. Similar to the present findings, T’Sjoen et al. have reported that circulating total testosterone levels were not associated with AMS scores in men with normal testosterone levels [33]. These results imply that another factor that is not testosterone levels is strongly associated with AMS scores in men with normal testosterone levels. In the present study, we demonstrated that aerobic capacity was associated with AMS scores in the cross-sectional study, and regular aerobic exercise improved AMS scores in the interventional study. These results suggest that aerobic capacity is strongly associated with aging-induced disorders than circulating testosterone levels in men with normal testosterone levels.

Recent studies have suggested that impaired male functions, namely, deterioration of male sexual function predicted aging-related diseases such as cardiovascular disease [34] or type 2 diabetes [35], and its risk factors [36,37]. Indeed, the AMS-sexual score significantly correlated to HbA1c levels in the present cross-sectional study. Additionally, the AMS-sexual score exhibited the strongest correlation with age among AMS scores. These results suggest that the AMS-sexual score is useful for predicting aging-related diseases or disorders in men.

The present study investigated the association between aerobic fitness and AMS scores in adult men and the effect of regular aerobic exercise on AMS scores in adult men. In the cross-sectional study, aerobic exercise capacity significantly correlated to the AMS scores in 169 adult men, after considering age and testosterone levels. In the interventional study, the 12-week regular aerobic exercise significantly decreased the AMS-sexual score and tended to reduce the AMS-total score. These results suggest that regular aerobic exercise is an effective strategy to improve aging-induced male-specific disorders. The present findings may provide a novel insight into the role of aerobic exercise to reduce the risk of aging-induced male-specific disorders and establish a novel treatment approach against aging in men.

Acknowledgements

We would like to thank the research members of S.M.’s laboratory at the University of Tsukuba for their technical assistance.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This work was supported by a grant-in-aid for Scientific Research KAKENHI from the Ministry of Education, Culture, Sports, Science, and Technology, Japan [15K12692 to S.M.]. H.K. is a recipients of a Grant-in-Aid for JSPS Fellow from the Japan Society for Promotion of Science.