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The Aging Male

ISSN: 1368-5538 (Print) 1473-0790 (Online) Journal homepage: https://www.tandfonline.com/loi/itam20

Regular aerobic exercise improves sexual


function assessed by the Aging Males’ Symptoms
questionnaire in adult men

Hiroshi Kumagai, Kanae Myoenzono, Toru Yoshikawa, Takehiko Tsujimoto,


Kosei Shimomura & Seiji Maeda

To cite this article: Hiroshi Kumagai, Kanae Myoenzono, Toru Yoshikawa, Takehiko Tsujimoto,
Kosei Shimomura & Seiji Maeda (2020): Regular aerobic exercise improves sexual function
assessed by the Aging Males’ Symptoms questionnaire in adult men, The Aging Male, DOI:
10.1080/13685538.2020.1724940

To link to this article: https://doi.org/10.1080/13685538.2020.1724940

Published online: 12 Feb 2020.

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THE AGING MALE
https://doi.org/10.1080/13685538.2020.1724940

ORIGINAL ARTICLE

Regular aerobic exercise improves sexual function assessed by the Aging


Males’ Symptoms questionnaire in adult men
Hiroshi Kumagaia,b,c, Kanae Myoenzonod, Toru Yoshikawae, Takehiko Tsujimotof, Kosei Shimomurad and
Seiji Maedaa
a
Division of Sports Medicine, Faculty of Health and Sport Sciences, University of Tsukuba, Tsukuba, Japan; bGraduate School of
Health and Sports Science, Juntendo University, Chiba, Japan; cJapan Society for the Promotion of Science, Tokyo, Japan;
d
Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Japan; eFaculty of Sports and Health Science,
Ryutsu Keizai University, Ryugasaki, Japan; fFaculty of Human Sciences, Shimane University, Matsue, Japan

ABSTRACT ARTICLE HISTORY


The leading cause of aging-induced male-specific disorders such as physical, mental and/or sex- Received 27 October 2019
ual symptoms is testosterone deficiency. Although aerobic exercise is suggested to improves cir- Accepted 29 January 2020
culating testosterone levels, physical fitness, depressive symptoms, and sexual function, the Published online 11 February
effect of regular aerobic exercise on aging-induced disorders has not yet been clarified. Here we 2020
performed cross-sectional and interventional studies to identify the effect of aerobic exercise on KEYWORDS
aging-induced disorders assessed by the Aging Males’ Symptoms questionnaire (AMS). In study Physical fitness; peak
1, the relationship between aerobic exercise capacity (i.e. peak oxygen consumption) and AMS oxygen consumption;
scores were cross-sectionally examined in 169 adult men. In study 2, the effect of a 12-week aerobic exercise;
regular aerobic exercise on AMS scores was longitudinally investigated in 18 adult men. In study testosterone; male sexual
1, the AMS-total, AMS-somatic, AMS-psychological, and AMS-sexual scores were significantly cor- function
related 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 effect-
ive strategy to improve aging-induced disorders in men.

Introduction depressive symptoms [21], and physical fitness [22,23].


Hence, improved aerobic fitness may be effective for
An aging-induced decrease in circulating testosterone
not only circulating testosterone levels but also aging-
levels adversely influences several functions such as
induced disorders in men. However, these possible
physical, psychological, and/or sexual functions [1–5]
and lowers the quality of life in men [6]. In clinical sit- associations among aerobic fitness and aging-induced
uations, the typical treatment for these disorders is disorders in men have not been fully clarified yet.
Here we hypothesized that aerobic exercise is pro-
testosterone replacement therapy, and it shows
positive effects on physical fitness, mood, and sexual tective against aging-induced disorders in men. To
function [7–11]. However, testosterone replacement confirm our hypothesis, we performed cross-sectional
therapy also has the potential risk for side effects in and interventional studies to identify the effect of aer-
men [12]. Therefore, it is preferable to establish an obic exercise on aging-induced disorders in men.
alternative treatment or a method that maximizes the
effect of testosterone supplementation on aging- Materials and methods
induced disorders in men.
Study design and participants
Previous studies have suggested that regular aer-
obic exercise improved circulating testosterone levels Study 1: cross sectional study
in healthy young, old, or overweight/obese men Participants were recruited through local newspaper
[13–18]. Besides, aerobic exercise is also associated advertisements and personal contacts. The inclusion
with improvements in sexual function [19,20], criteria were as follows: (1) men; (2) age 20 years.

CONTACT Seiji Maeda maeda.seiji.gn@u.tsukuba.ac.jp Division of Sports Medicine, Faculty of Health and Sport Sciences, University of Tsukuba,
Tsukuba, Ibaraki305-8574, Japan
ß 2020 Informa UK Limited, trading as Taylor & Francis Group
2 H. KUMAGAI ET AL.

The exclusion criteria for the present study were as Ltd., Kyoto, Japan). Participants were asked to wear
follows: (1) under 35 years old; (2) presence or history the accelerometer on a belt over their hip both for 2
of cardio/cerebrovascular disease (e.g. angina, myocar- weeks prior to the aerobic exercise intervention
dial infarction, and stroke) assessed using a medical (before intervention) and in the last 2 weeks of the
history questionnaire; (3) currently receiving medica- aerobic exercise intervention period (after interven-
tions for erectile dysfunction (ED) or depression; (4) tion) and to wear the device at all times while they
current smokers. In addition, participants who took were awake except when swimming or bathing. For
meals and/or medications on the morning of the data reduction, a valid day was defined as 10 or more
measurement were excluded. A total of 168 adult men h/day of monitor wear. The PA time was classified as
were included in the analyses; median [interquartile follows: light-intensity physical activity (LPA), 1.6–2.9
range] of age was 62 [53–69] years old. The number metabolic equivalents (METs); moderate-intensity phys-
of participants who were regularly using antihyperten- ical activity (MPA), 3.0–5.9 METs; vigorous-intensity
sive medication, antidyslipidemic medication, and physical activity (VPA), 6.0 METs; and moderate to
hypoglycemic medication were 20 (11.8%), 14 (8.3%), vigorous-intensity physical activity (MVPA).
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 Aging Males’ Symptoms questionnaire (AMS)
Declaration, and all participants provided written The AMS is a self-answer type questionnaire and
informed consent before inclusion in the study. which assesses aging-induced male specific disorders.
The AMS is consists of 17 items, including five psycho-
Study 2: regular aerobic exercise
logical symptoms score items (questions 6–8, 11 and
Participants were recruited through local newspaper
13), seven somatic symptoms score items (questions
advertisements. The inclusion criteria were as follows:
1–5, 9 and 10), and five sexual symptoms score items
(1) men; (2) age 30–64 years. The exclusion criteria for
(questions 12 and 14–17) [28,29]. Each item is eval-
the present study were as follows: (1) under 35 years
uated with five phases, from 1 point (no symptoms) to
old; (2) presence or history of cardio/cerebrovascular
5 points (very severe symptoms) and the range of
disease (e.g. angina, myocardial infarction, and stroke)
total scores is 17–85. Severity is classified into four
assessed via a medical history questionnaire. Initially,
groups based on the range of scores: 17–26 points as
24 men were enrolled in this study, but three were
no/low symptoms, 27–36 points as mild symptoms,
excluded under 35 years old and other three were
37–49 points as moderate symptoms, and 50–85
excluded due to a lack of post-training data (n ¼ 1,
relocated; n ¼ 1, time; and n ¼ 1, personal issues). A points as severe symptoms.
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 Aerobic exercise capacity
the institutional review board of the University of
Tsukuba. All study procedures and potential risks were To measure aerobic exercise capacity as an index of
explained to the participants and they provided writ- exercise endurance, the subjects performed peak oxy-
ten informed consent to participate in the study. This gen consumption. To evaluate their aerobic exercise
study 2 was a pre-specified sub-study (secondary ana- capacity, the subjects performed an incremental
lysis) of UMIN000027711 [24]. cycling ergometer exercise consisting of 2 min at 20 W
Subjects participated in an aerobic exercise class for followed by a 10–20 W increase every one minutes.
up to 90 min/day, 3 times/week for 12 weeks as previ- Aerobic exercise capacity was measured using an
ously described [13,22,25–27]. The exercise program online computer-assisted circuit spirometry (AE300S;
included a 15–20 min warm-up session followed by an Minato Medical Science, Osaka, Japan) and peak oxy-
approximately 40–60 min walking and/or light jogging gen consumption was assumed when at least two of
session, and concluded with a 15–25 min cool-down the following criteria were satisfied: (1) the participant
session. Daily steps and physical activity time in both reaching their age-predicted maximal HR (i.e.
the aerobic exercise sessions and free-living conditions 220  age), (2) Borg scale >19, (3) respiratory equiva-
were assessed using a tri-axial accelerometer lent >1.2, or (4) the participant being unable to main-
(ActiveStyle Pro HJA-750IT; Omuron Healthcare Co. tain a pedaling speed <55 rpm [20].
THE AGING MALE 3

Anthropometric measurements Table 1. Characteristics of studied men (n ¼ 169).


Variable n ¼ 169
Body weight was measured to the nearest 0.1 kg using
Age, years 60 ± 12
a digital scale. Height was measured to the nearest Height, cm 167.3 ± 6.7
0.1 cm using a wall-mounted stadiometer. Body mass Body mass, kg 64.6 ± 10.1
BMI, kg/m2 23.0 ± 3.1
index (BMI) was calculated as the participants’ weight Waist circumference, cm 82.9 ± 9.9
(kg) divided by their height (m2). Waist circumference Visceral fat area, cm2 64.1 ± 31.0
HDL cholesterol, mg/dl 65 ± 16
was directly measured on the skin at the level of the LDL cholesterol, mg/dl 126 ± 32
umbilicus with the participant in a standing position; Triglycerides, mg/dl 101 ± 43
Glucose, mg/dl 104 ± 20
measurements were made in duplicate to the nearest HbA1c, mg/dl 5.6 ± 0.6
0.1 cm. Visceral fat area was measured using the dual- Testosterone, nmol/l 20.3 ± 6.5
Aerobic exercise capacity, ml/min/kg 26.7 ± 7.4
impedance analysis method (HSD-2000; Omron AMS-total score, points 29 ± 8
Healthcare, Kyoto, Japan). 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].
Blood biochemistry BMI: body mass index; HDL: high-density lipoprotein; LDL: low-density
lipoprotein; AMS: Aging Males’ Symptoms.
Blood samples were taken in the morning after 12-h Aerobic exercise capacity was assessed by peak oxygen consumption.
overnight fast. Serum concentrations of triglyceride,
total cholesterol, high-density lipoprotein (HDL) chol- Table 2. Relationships between each variable.
esterol, low-density lipoprotein (LDL) cholesterol, and AMS-total AMS-som AMS-psy AMS-sex
plasma concentration of glucose and HbA1c were Age, years 0.152 0.049 0.197 0.396
determined using standard enzymatic techniques. Height, cm 0.194 0.084 0.012 0.252
BMI, kg/m2 0.032 0.073 0.068 0.070
Serum total testosterone levels were measured using Visceral fat area, cm2 0.010 0.100 0.088 0.041
chemiluminescent immunoassay by commercial HDL cholesterol, mg/dl 0.069 0.075 0.099 0.111
LDL cholesterol, mg/dl 0.165 0.114 0.021 0.198
laboratory (LSI medience. Ibaraki, Japan). 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
Statistical analysis Testosterone, nmol/l 0.067 0.011 0.091 0.066
BMI: body mass index; HDL: high-density lipoprotein; LDL: low-density
The Shapiro–Wilk test was used to assess the normal- lipoprotein; VO2peak: peak oxygen consumption; AMS-total: aging male
symptoms-total; AMS-som: aging male symptoms-somatic; AMS-psy:
ity of all parameters. Data are expressed as the mean- aging male symptoms-psychological; AMS-sex: aging male symptoms-
s ± standard deviation (SD) or frequency counts (for sexual.
p < 0.01; p < 0.05.
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 LDL cholesterol (125 mg/dl), triglycerides (92 mg/dl),
assess the group differences between data before and glucose (101 mg/dl), and testosterone (19.8 nmol/l)
after the 12-week regular aerobic exercise. The rela- were within the normal range.
tionships among each parameter were analyzed using Table 2 shows the correlations between each variable.
Spearman’s (rs) correlation coefficient. Independent Age was significantly correlated with the scores of AMS-
correlates of AMS scores were examined by using a total (rs ¼ 0.152, p < 0.05), AMS-psychological
multivariate linear regression analysis (independent (rs ¼ 0.197, p < 0.05), and AMS-sexual (rs ¼ 0.396,
variables: age, aerobic exercise capacity and testoster- p < 0.01) (Table 2). Aerobic exercise capacity was signifi-
one levels). Statistical significance was set a priori at cantly correlated with the scores of AMS-total
p < 0.05 for all comparisons. Statistical analyses were (rs ¼ 0.287, p < 0.01), AMS-somatic (rs ¼ 0.227,
performed using JMP Pro version 12 (SAS Institute). p < 0.01), and AMS-sexual (rs ¼ 0.309, p < 0.01) (Figure
1). On the other hand, serum testosterone levels were
Results not significantly correlated with AMS scores (Table 2).
After considering age and circulating testosterone levels,
Study 1
aerobic exercise capacity was significantly associated
The characteristics of the studied subjects are sum- with AMS-total (b ¼ 0.347, p < 0.01), AMS-somatic
marized in Table 1. Medians of BMI (22.5 kg/m2), waist (b ¼ 0.370, p < 0.01), AMS-psychological (b ¼ 0.225,
circumference (82.0 cm), HDL cholesterol (62 mg/dl), p < 0.05) and AMS-sexual (b ¼ 0.223, p < 0.01).
4 H. KUMAGAI ET AL.

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

Study 2 and the effect of regular aerobic exercise on the AMS


scores in adult men. In the cross-sectional study, aerobic
Table 3 shows the characteristics of subjects before and
fitness was significantly associated with AMS scores in
after the 12-week aerobic exercise intervention. Body
169 adult men after considering age and testosterone
mass, BMI, waist circumference, and visceral fat area sig-
levels. Furthermore, in the interventional study, the 12-
nificantly decreased, and physical activity levels and aer-
week regular aerobic exercise significantly decreased
obic exercise capacity significantly increased after the
the AMS-sexual score and tended to decrease the AMS-
aerobic exercise intervention. On the other hand, aerobic
total score. These results suggest that regular aerobic
exercise training tended to increase serum testosterone
exercise is an effective strategy to improve AMS scores,
levels. Figure 2 shows the AMS scores before and after
especially sexual function in adult men.
the intervention. The 12-week regular aerobic exercise
The AMS questionnaire is used for the assessment of
significantly decreased the AMS-sexual score and tended
aging-induced disorders such as somatic, psychological,
to reduce the AMS-total score, but not the AMS-somatic
and sexual functions in men. Several studies have sug-
and AMS-psychological scores (Figure 2). Although, the
percentage change in serum testosterone levels did not gested that aerobic exercise associated with sexual func-
correlate to AMS scores, the percentage change in VPA tion [19,20], depressive symptoms [21], and physical
significantly correlated to that in AMS-sexual score fitness [22,23], implying aerobic exercise effective for
(rs ¼ 0.539, p < 0.05). AMS scores. Thus, the present study hypothesized that
regular aerobic exercise was associated with AMS scores.
In the cross-sectional study, high aerobic exercise cap-
Discussion
acity was associated with low scores of the AMS-total,
In the present study, we investigated the association AMS-somatic, AMS-psychological, and AMS-sexual after
between aerobic fitness and AMS scores in adult men, considering age and serum testosterone levels in adult
THE AGING MALE 5

Table 3. Characteristics of subjects before and after the aerobic exercise intervention.
n ¼ 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/m2 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, cm2 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: moder-
ate 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.

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.

men. Additionally, the 12-week regular aerobic exercise AMS-somatic and AMS-psychological scores. Taken
significantly decreased the AMS-sexual score and tended together, regular aerobic exercise is effective to improve
to reduce the AMS-total score in the interventional in aging-induced disorders, especially AMS-sexual and
study. Although there were no significant reductions in AMS-total scores. These findings propose a new option
the AMS-somatic and AMS-psychological scores, the (i.e. regular exercise) for prevention and treatment for
average values of these decreased after the 12-week aging-induced disorders in men.
intervention. It is possible that the duration of the In clinical situations, testosterone replacement ther-
exercise intervention was not enough to improve apy is a typical treatment strategy for aging-induced
6 H. KUMAGAI ET AL.

disorders such as physical, psychological, and/or sex- and the effect of regular aerobic exercise on AMS
ual functions in men [7–11]. However, testosterone scores in adult men. In the cross-sectional study, aer-
replacement therapy also has the potential risk of obic exercise capacity significantly correlated to the
negative effects on health [12]. Therefore, it is neces- AMS scores in 169 adult men, after considering age
sary to establish a way to maximize the effect of mod- and testosterone levels. In the interventional study,
est testosterone supplementation in men. Several the 12-week regular aerobic exercise significantly
studies have demonstrated that a combination of tes- decreased the AMS-sexual score and tended to reduce
tosterone replacement therapy and exercise had sig- the AMS-total score. These results suggest that regular
nificant improvements in circulating testosterone aerobic exercise is an effective strategy to improve
levels, total AMS score, the International Index of aging-induced male-specific disorders. The present
Erectile Function score, and body compositions com- findings may provide a novel insight into the role of
pared to testosterone replacement therapy alone aerobic exercise to reduce the risk of aging-induced
[30–32]. These previous studies suggested the import- male-specific disorders and establish a novel treatment
ance of exercise for the treatment of aging-induced approach against aging in men.
disorders in terms of the combination of testosterone
replacement therapy and exercise.
Aging-induced male-specific disorders are sug- Acknowledgements
gested to be caused by a decrease in circulating We would like to thank the research members of S.M.’s
testosterone levels that occurs with aging [1–5]. laboratory at the University of Tsukuba for their technical
However, in the present cross-sectional study, no sig- assistance.
nificant associations were found between serum total
testosterone levels and AMS scores in men with nor- Disclosure statement
mal testosterone levels. Besides, changes in serum
No potential conflict of interest was reported by the
total testosterone levels did not correlate to AMS author(s).
scores in the present interventional study. Similar to
the present findings, T’Sjoen et al. have reported that
circulating total testosterone levels were not associ- Funding
ated with AMS scores in men with normal testoster- This work was supported by a grant-in-aid for Scientific
one levels [33]. These results imply that another factor Research KAKENHI from the Ministry of Education, Culture,
that is not testosterone levels is strongly associated Sports, Science, and Technology, Japan [15K12692 to S.M.].
H.K. is a recipients of a Grant-in-Aid for JSPS Fellow from the
with AMS scores in men with normal testosterone lev-
Japan Society for Promotion of Science.
els. In the present study, we demonstrated that aer-
obic capacity was associated with AMS scores in the
cross-sectional study, and regular aerobic exercise
improved AMS scores in the interventional study. References
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