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Sistema de Información Científica
Red de Revistas Científicas de América Latina y el Caribe, España y Portugal
Nutrición
Hospitalaria
Nutr Hosp. 2017; 34(3):608-612 ISSN 0212-1611 - CODEN NUHOEQ S.V.R. 318
Trabajo Original
Obesidad y síndrome metabólico
Correspondence:
Manuel Rosety Rodríguez. Department of Medicine.
Universidad de Cádiz. Plaza Falla, 9. 11003 Cádiz,
Spain
e-mail: manuel.rosetyrodriguez@uca.es
Rosety MA, Díaz A, Rosety JM, Pery MT, Brenes-Martín F, Bernardi M, García N, Rosety-Rodríguez M,
Ordóñez FJ, Rosety I. Exercise improved semen quality and reproductive hormone levels in sedentary
obese adults. Nutr Hosp 2017;34:608-612
Exercise improved semen quality and reproductive hormone levels in sedentary
obese adults
Mejora de calidad seminal y perfi l hormonal en adultos obesos sedentarios mediante ejercicio
Miguel Ángel Rosety
1
, Antonio Díaz
2
, Jesús María Rosety
3
, M.ª Teresa Pery
2
, Francisco Brenes-Martín
2
, Marco Bernardi
4
,
Natalia García
5
, Manuel Rosety-Rodríguez
2
, Francisco Javier Ordóñez
6
and Ignacio Rosety
7
Departments of
1
Physical Education,
2
Medicine,
5
Pathological Anatomy and
7
Human Anatomy. Universidad de Cádiz. Cádiz, Spain.
3
Urology Service. Hospital Puerta del Mar.
Universidad de Cádiz. Cádiz, Spain.
4
School of Sport Medicine. University of Rome La Sapeinza. Rome, Italy.
6
School of Sport Medicine. Universidad de Cádiz.
Cádiz, Spain
Key words:
Obesity. Aerobic
training. Semen.
Testosterone.
Palabras clave:
Obesidad.
Entrenamiento
aeróbico. Semen.
Testosterona.
Resumen
Introducción:
cada vez existe un mayor nivel de evidencia sobre el impacto negativo de la obesidad en la calidad seminal. Sin embargo, la utilidad
del ejercicio en este grupo de pacientes ha recibido escasa atención. El presente estudio pretende determinar la infl uencia de un programa de
entrenamiento aeróbico en la calidad seminal de adultos obesos.
Material y métodos:
noventa adultos varones se asignaron aleatoriamente al grupo experimental (n = 45) o control (n = 45). El grupo experi-
mental desarrolló un programa de entrenamiento aeróbico en tapiz rodante de 16 semanas con tres sesiones/semana. Cada sesión se estructuró
en calentamiento (10-15 minutos), 35-50 minutos en tapiz rodante (incrementando cinco minutos/cuatro semanas) a una intensidad del 50-65%
de su frecuencia cardiaca máxima (incrementando 5%/cuatro semanas) y vuelta a la calma (5-10 minutos). La calidad seminal se evaluó mediante
determinación de volumen seminal, concentración espermática, así como porcentajes de motilidad y morfología normal según criterios de la
Organización Mundial de la Salud (OMS). Los niveles séricos de las hormonas folículo estimulante (FSH), luteinizante (LH) y testosterona se
determinaron mediante ELISA. También se evaluó la composición corporal y condición física de los participantes.
Resultados:
tras fi nalizar el entrenamiento, la concentración, la motilidad y la normal morfología se incrementaron signifi cativamente. Asimismo,
se observó una mejoría de los niveles de testosterona. Finalmente, se observaron correlaciones estadísticamente signifi cativas entre parámetros
seminales y marcadores de masa grasa abdominal.
Conclusión:
el ejercicio aeróbico mejoró la calidad seminal de adultos obesos sedentarios. Estos resultados podrían explicarse, al menos en
parte, por la mejora del perfi l hormonal de los participantes.
Abstract
Introduction:
From the previously published literature on the relationship between obesity and infertility, it is clear that male obesity negatively
impacts semen quality. Accordingly, this study was conducted to determine whether regular exercise may improve semen quality in sedentary
obese adults.
Material and methods:
Ninety obese adults were randomly allocated to the intervention (n = 45) or control group (n = 45). Participants in the
intervention group performed a 16-week aerobic training program in a treadmill, three sessions per week, consisting of a warm-up (10-15 minutes),
35-50 minutes treadmill exercise (increasing fi ve minutes per four weeks) at a work intensity of 50-65% of peak heart rate (increasing a 5% per
four weeks) and cooling-down (5-10 minutes). Semen quality assessment included semen volume, sperm concentration and the percentages
of progressive motility and normal morphology. Serum levels of follicle-stimulating hormone (FSH), luteinizing hormone (LH), testosterone and
estradiol were determined by ELISA. Body composition and physical fi tness were also assessed.
Results:
After the completion of the training program, sperm count, motility and normal morphology were signifi cantly increased. A second key
fi nding was that exercise improved reproductive hormone levels by increasing serum testosterone. Lastly, signifi cant correlations were found
between seminal outcomes and abdominal obesity.
Conclusion:
A short-term intervention program based on aerobic training improved semen quality in sedentary obese adults. This fi nding may
be explained, at least in part, by an improvement of the reproductive hormone profi le.
Received: 15/09/2016
Accepted: 26/09/2016
609
EXERCISE IMPROVED SEMEN QUALITY AND REPRODUCTIVE HORMONE LEVELS IN SEDENTARY OBESE ADULTS
[
Nutr Hosp 2017;34(3):608-612
]
INTRODUCTION
There is emerging evidence that male obesity negatively
impacts fertility (1,2). In this respect, in a multivariate analysis
conducted by Bener et al. (3), patients having a body mass index
(BMI) > 30 were found to have a three-fold increased risk of
infertility. In a more detailed way, Hammiche et al. (2)
found sperm
concentration and total motile sperm count in men of subfertile
couples were detrimentally affected by a high central adiposity.
Lastly, a systematic review of the literature also concluded over-
weight and obesity were associated with an increased prevalence
of azoospermia or oligozoospermia (4).
Several hypotheses have been proposed to explain the patho-
logical mechanisms underlying this association. Recent studies
have found that excess adipose tissue has a negative impact
on reproductive hormone levels such as testosterone (5). Fur-
thermore, given that human spermatogenesis is highly sensitive
to heat (6), raised gonadal heat resulting from increased scrotal
adiposity might be associated with reduced sperm function and
subfertility. Lastly, a relationship between obesity and increased
sperm oxidative stress was also reported by Fariello et al. (7).
Fortunately, a recent animal study has found that simple diet
and exercise interventions can be used to reverse the damaging
effects of obesity on sperm function (8).
However, to date, no intervention studies have been focused on
reversing these deleterious effects by regular exercise, despite
recent observational studies showed that physically active sub-
jects seemed to have a more anabolic hormonal environment and
a healthier semen production (9). The lack of information in the
literature may be explained, at least in part, given that previous
studies suggested a negative impact of some types of exercise
on semen quality (10,11). Fortunately, a recent study concluded
that physical activity was not deleterious to testicular function in
young healthy adults (12).
For the reasons already mentioned, it was hypothesized that
aerobic training could improve semen quality. Accordingly, the
main objective was to determine the effect of a short-term aero-
bic training program on semen quality and reproductive hormone
profile in sedentary obese adults.
MATERIALS AND METHODS
PARTICIPANTS
Ninety adults with obesity volunteered for this longitudinal study
from the community. Characteristics of participants at baseline
are summarized in table I. All subjects met the following inclusion
criteria: a) young adults (25-40 years); b) obese, defined as a
BMI ≥ 30 kg/m
2
as was suggested for reproductive endocrinology
research (13); and c) medical approval after completing a pre-par-
ticipation physical examination.
On the other hand, exclusion criteria were: a) participation in
a training program in the six months prior to their participation
in the trial; b) testicular varicocele and/or genital infection, leu-
kocytospermia, chronic illness and serious systemic diseases; c)
previous surgery (e.g., vasectomy reversal, varicocele removal,
etc.); d) receiving medication and/or antioxidant consumption that
may interfere with the redox homeostasis; and e) toxic habits
(smoking and/or alcohol).
Participants were randomly allocated to the intervention (n =
45) or control group (n = 45) using a concealed method.
This research has been conducted in full accordance with ethi-
cal principles, including the World Medical Association Declaration
of Helsinki (version 2002). Participants gave their written informed
consent prior to study participation. Furthermore, this protocol was
approved by an Institutional Ethics Committee.
INTERVENTION PROGRAM
Participants in the intervention group performed a 16-week
aerobic training program in a treadmill, three sessions per week,
consisting of a warm-up (10-15 minutes), 35-50 minutes tread-
mill exercise (increasing five minutes each four weeks) at a work
intensity of 50-65% of peak heart rate (increasing a 5% each
four weeks) measured during a maximal treadmill test, and cool-
ing-down (5-10 minutes). In order to ensure that the training
workload was appropriate, all participants from the intervention
group wore a wireless wearable heart rate monitor (Sport Tester
PE3000, Polar Electro, Kempele, Finland).
SEMEN ANALYSIS
Semen was collected after three days of ejaculation abstinence
(verified by self-report on the day of sample collection) by manual
masturbation into a sterile container on site and examined within
Table I.
Characteristics of sedentary
obese adults enrolled in the intervention
(n = 45) and control (n = 45) groups
Intervention
Control
p value
Age (years)
36.3 (3.2)
35.6 (3.5)
0.664
Fat mass (%)
34.6 (3.6)
33.8 (3.8)
0.479
BMI (kg/m
2
)
31.2 (1.1)
30.9 (0.8)
0.341
WC (cm)
107.6 (5.3)
106.8 (5.7)
0.265
c-HDL (mg/dl)
177.9 (14.6)
174.2 (15.2)
0.383
c-HDL (mg/dl)
38.3 (1.9)
40.0 (2.3)
0.206
Triglycerides (mg/dl)
168.4 (13.6)
165.8 (14.1)
0.410
Glycaemia (mg/dl)
109.4 (5.8)
106.1 (6.2)
0.242
Daily energy intake (kcal)
2394 (172)
2308 (185)
0.568
Fitness (ml/kg/min)
27.8 (1.7)
28.4 (1.9)
0.211
Results expressed as mean (SD). BMI: Body mass index; WC: Waist
circumference; c-HDL: High density lipoprotein cholesterol; SBP: Systolic
blood pressure; DBP: Diastolic blood pressure.
610
M. Á. Rosety et al.
[
Nutr Hosp 2017;34(3):608-612
]
30 minutes of ejaculation. It should be pointed out that within
this time it has been shown that sperm motility is stable (14).
Semen quality assessment included semen volume (ml), sperm
concentration (%), sperm motility (%) and normal morphologic
features (%). All parameters were examined out according to
the World Health Organization (WHO) guidelines (15) by trained
laboratory technicians. A 1-ml sample was diluted (1:20) with
formaldehyde to examine the sperm concentration by hemocy-
tometer (Hauser Scientific Inc., Horsham, PA). The progressive
sperm motility percentage was measured using the known volume
of the specimen, which was placed onto a clean glass slide and
covered by a coverslip, and examined under positive phase-con-
trast microscopy at a magnification of ×400 with the help of an
ocular grid. For morphological classification, 100 spermatozoa
were counted using a high-quality phase-contrast microscope
(magnification ×600). Thin, well-spread smears were air-dried,
fixed, and stained according to the Papanicolaou method. The
classification, including head shape/size defects, neck and mid-
piece defects, tail defects, and cytoplasmic droplets, was based
on the manual published by the WHO.
SERUM REPRODUCTIVE HORMONES
Blood samples (5 ml) were collected from the antecubital vein
after a 12-h fast (08.00-09.00 a.m.). The whole blood was cen-
trifuged at 3,000 rpm for ten minutes. The plasma was separated
and stored at -80 °C until further analysis. Serum levels of folli-
cle-stimulating hormone (FSH), luteinizing hormone (LH), estradiol
and testosterone were determined by ELISA (Diagnostics Systems
Laboratories Inc., Texas, USA).
BODY COMPOSITION AND PHYSICAL FITNESS
Regarding anthropometric assessment, fat free mass percentage
was assessed by bioelectrical impedance analysis (MC-180, Tanita
Ltd., UK). Participants were requested to not perform moderate or
vigorous exercise for 24 hours prior to testing as well as to abstain
from eating or drinking for two hours before testing. Moreover, they
were asked to urinate immediately prior to data collection. The fol-
lowing equation was used to calculate the body mass index (BMI
= weight [kg]/height [m]
2
) being expressed as kg/m
2
. Height was
determined with an accuracy of 0.1 cm by precision stadiometer.
Body weight was assessed with an accuracy of 0.1 kg using an
electronic balance. Lastly, waist circumference (WC) was measured
as halfway between the costal edge and the crista.
In order to determine physical fitness, all participants (n = 90)
performed a continuous maximal incremental test, using the stan-
dard Bruce treadmill protocol, until exhaustion. Gas exchange data
were collected throughout the test using a breath by breath met-
abolic system. The electrocardiograms (ECGs) were continuously
recorded using a 12 lead stress analysis system. In this respect,
the criteria used to determine the maximal oxygen consumption
(VO
2
max) was the maximal O
2
value at plateau despite increasing
workload (< 2 ml/kg/min increase in VO
2
between progressive
stages). Furthermore, it should be pointed out that all participants,
including the control group, underwent a pre-training period to be
familiarized with the correct use of the treadmill.
NUTRITIONAL INTAKE RECORD
To control the potential confounding effect of diet, participants
included in intervention and control groups recorded their nutri-
tional intake for seven days. Participants were instructed about
completion of the nutritional protocol.
STATISTICAL ANALYSIS
The results of biochemical and anthropometric assessments
were expressed as mean (SD). Given the limited sample size, the
Shapiro-Wilk test was used to assess whether data were normally
distributed. To compare the mean values, repeated one-way anal-
ysis of variance (ANOVA), with post hoc Bonferroni correction to
account for multiple tests, were used. Regarding semen quality
and reproductive hormone assessments, results were expressed
as median (5-95
th
percentiles). The Mann-Whitney U test was
used to compare differences between the intervention and con-
trol groups. Spearman’s coefficient was used to identify correla-
tions among tested parameters. The significance of the changes
observed was ascertained to be p < 0.05.
RESULTS
Physical fitness, expressed as VO
2
max, was significantly
improved (27.8 ± 1.7
vs
30.6 ± 1.4 ml/kg/min; p = 0.0371)
in the intervention group. Body composition was improved as fat
mass percentage was significantly reduced (34.6 ± 3.2
vs
32.1
± 3.0%; p = 0.0322). Similarly, WC was significantly decreased
after being exercised (107.6 ± 5.3
vs
104.1 ± 4.7; p = 0.0438).
When compared to pre-test, sperm concentration (p = 0.032),
progressive sperm motility (p = 0.021) and
normal morphology per-
centages (p = 0.026) were significantly improved after the completion
of the training program. On the other hand, no significant changes
were observed in semen volume in the intervention group.
Regarding reproductive hormone profile, the ratio testosterone/
estradiol was significantly improved (p = 0.002). In addition, it was
found testosterone level was significantly increased (p = 0.037)
after being exercised. These results are summarized in table II.
Furthermore, negative significant correlations were found between
WC and both sperm concentration (r = -0.32; p = 0.028) and pro-
gressive sperm motility (r = -0.29; p = 0.036) in the intervention
group. Similar results were found between WC and testosterone
levels (r = -0.38; p = 0.017) after being exercised.
Lastly, no significant differences were found between the inter-
vention and control groups when assessing energy intake (2,394
± 172
vs
2,306 ± 188 kcal; p = 0.316) and mean daily vitamin
611
EXERCISE IMPROVED SEMEN QUALITY AND REPRODUCTIVE HORMONE LEVELS IN SEDENTARY OBESE ADULTS
[
Nutr Hosp 2017;34(3):608-612
]
intake (9.2 ± 1.8
vs
9.6 ± 2.1 mg/d vitamin E, p = 0.512; 79.7
± 18.2
vs
81.4 ± 20.6 mg/d vitamin C, p = 0.431).
No significant changes in any of the tested parameters were
found in the control group (Table III). Finally, it should be also
pointed out that neither sports-related injuries nor withdrawals
from the program were reported during the entire study period.
DISCUSSION
The most striking finding was that aerobic training improved
semen quality in sedentary obese adults. Similarly, Gaskins et al. (16)
demonstrated that higher physical activity and less TV watching
were significantly associated with higher total sperm count and
sperm concentration in young healthy men. However, it should be
pointed out when designing a training protocol that, depending on
sport modality and/or intensity, physical activity may impact in a
positive or negative way on semen quality. In this respect, bicycling
≥ 5 h/week was associated with lower sperm concentration and
motility (17). Likewise, long-term strenuous treadmill exercises
(80% VO
2
max) have a deleterious effect on reproduction (11).
Lastly, physical exercise at high altitude was associated with a
testicular dysfunction leading to a reduced sperm concentration
in non-obese mountaineers (10).
Despite neither antioxidants nor markers of oxidative damage
in seminal plasma were assessed in the present study, it may
be hypothesized that the reduction of oxidative damage induced
by aerobic training may explain, at least in part, the improve-
ment of semen quality, mainly if we take into consideration a
similar intervention program based on aerobic training increased
antioxidant system and reduced oxidative damage in adults with
type 2 diabetes mellitus (18). Similarly, Tartibian and Maleki (19)
found that spermatozoa from recreationally active men may be
less susceptible to oxidative stress-induced DNA damage and
hence infertility.
Previous studies have concluded that the reduction in semen
quality found in men with BMI > 25 kg/m
2
could be explained,
at least in part, by an increased serum estradiol level (20). The
current study also showed reproductive hormone profile was
improved after the completion of the training program. The sig-
nificant reduction of fat mass after the completion of the training
program may play a key role supporting this finding (21). Consis-
tent with these results, aerobic training at moderate intensity for
24-weeks significantly increased testosterone level in abdominally
obese adults (22). It should be emphasized that our intervention
program lasted just 16 weeks so that it may be considered to be
more feasible and practical for participants. Lastly, it should be
noted that participants remained overweight or obese after the
completion of the training program. This could explain why we did
not observe a larger improvement in the reproductive hormonal
profile, as was previously reported by Hakonsen et al. (21).
Another challenge of the present study was to identify signifi-
cant associations between semen characteristics and anthropo-
metric parameters in order to provide an easier, quicker, cheaper
assessment of the seminal outcomes. In this line, negative sig-
nificant correlations were found between WC and both sperm
count and progressive motility, thus confirming that abdominal
fat impairs semen quality (2,23). Conversely, it should be pointed
out that Eskandar et al. (24) did not find any significant correlation
between BMI and semen quality parameters in men seeking fertil-
ity treatment. However, they did not assess any indices of central
fat distribution, such as WC and/or hip circumference, to confirm
their results. Similarly, a systematic review with meta-analysis
revealed little evidence for a relationship with semen parameters
and increased BMI (25). The latter authors also concluded the
main limitation of this review was that data from most studies
could not be aggregated for meta-analysis (25).
Table II.
Semen quality and serum
reproductive hormone profile in
sedentary obese adults enrolled in the
intervention (n = 45) group
Pre-test
Post-test
p value
Volume
2.81 (0.89-6.2)
2.92 (1.12-6.5)
0.182
Concentration
45.0 (4.7-296.4)
48.8 (5.3-312.8)
0.040
Progressive motility
42.6 (9.0-56.8)
46.2 (10.2-60.0)
0.015
Morphology
21.0 (2.7-61.8)
23.3 (3.9-64.6)
0.028
LH
4.46 (0.76-10.3)
4.58 (0.81-9.9)
0.094
FSH
5.33 (1.52-21.8)
5.57 (1.47-20.6)
0.166
Testosterone
4.36 (2.88-24.6)
4.78 (3.62-25.1)
0.036
Estradiol
56.3 (41.6-69.8)
54.9 (40.1-68.7)
0.220
Results expressed as median (5-95
th
percentiles). Volume: semen volume
expressed as ml. Sperm concentration expressed as 10
6
/ml. Progressive
sperm motility and normal morphology expressed as percentages (%).
FSH and LH expressed mIU/ml. Testosterone expressed as ng/ml. Estradiol
expressed as pg/ml.
Table III.
Seminal outcomes and serum
reproductive hormone profile in
sedentary obese adults enrolled in the
control group (n = 45)
Baseline
Final
p value
Volume
2.71 (0.94-6.11)
2.64 (0.88-5.98)
0.12
Concentration
43.2 (4.1- 306.8)
42.8 (3.8-301.4)
0.36
Progressive motility
41.2 (8.4-50.6)
40.4 (8.2-52.8)
0.44
Morphology
20.3 (2.4-61.2)
19.4 (2.1-60.5)
0.08
LH
4.60 (0.98-10.7)
4.72 (1.12-11.1)
0.31
FSH
5.82 (1.76-22.3)
6.02 (1.90-24.1)
0.26
Testosterone
4.34 (2.46-23.7)
4.18 (2.39-23.0)
0.54
Estradiol
57.9 (42.8-70.6)
58.4 (43.3-72.1)
0.18
Results expressed as median (5-95
th
percentiles). Volume: semen volume
expressed as ml. Sperm concentration expressed as 10
6
/ml. Progressive
sperm motility and normal morphology expressed as percentages (%).
FSH and LH expressed mIU/ml. Testosterone expressed as ng/ml. Estradiol
expressed as pg/ml.
612
M. Á. Rosety et al.
[
Nutr Hosp 2017;34(3):608-612
]
This study had some limitations and strengths. The major weak-
ness was the relatively short duration of the exercise interven-
tion, so that there was no follow-up to determine whether these
positive effects induced by aerobic training were maintained. In
addition, the short sample size may also limit the generalization
of the results.
Strengths of the present study included the excellent adher-
ence, rate suggesting the training program was effective and easy
to follow up. Secondly, the majority of studies previously report-
ed were originated from fertility clinics, where patient cohorts
are frequently biased toward, sub-fertile men, which may also
confound findings. Thirdly, some studies rely on self-reporting
of parameters such as lifestyle factors and BMI, which can lead
to under reporting (8). Lastly, given that spermatogenesis takes
approximately 64 days (26), the follow-up period in the present
study (112 days) should be able to detect any change induced by
the intervention program.
Finally, it was concluded that: a) aerobic training improved
semen quality in obese sedentary adults; and b) this finding could
be explained, at least in part, by an improvement of the repro-
ductive hormone profile after the completion of the intervention
program.
There is a clear need for long-term, well-conducted studies to
determine whether correction of semen quality induced by exer-
cise improves the outcomes of live birth and pregnancy rate in
obese adults.
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