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Response of semen parameters to three training
modalities
Diana Vaamonde, Ph.D.,
a
Marzo Edir Da Silva-Grigoletto, Ph.D.,
b
Juan Manuel Garc
ıa-Manso,
Ph.D.,
c
Ricardo Vaamonde-Lemos, M.D., Ph.D.,
a
Robert James Swanson, Ph.D.,
d
and
Sergio Carlos Oehninger, M.D., Ph.D.
e
a
Morphological Sciences Department, School of Medicine, University of C
ordoba, C
ordoba, Spain;
b
Andalusian Center of
Sports Medicine, C
ordoba, Spain;
c
Physical Education Department, School of Physical Activity and Sport Sciences,
University of Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, Spain;
d
Department of Biological Sciences, Old
Dominion University and Eastern Virginia Medical School, Norfolk, Virginia; and
e
the Jones Institute for Reproductive
Medicine, Department of Obstetrics and Gynecology, Eastern Virginia Medical School, Norfolk, Virginia
Objective: To investigate the effect of different training modalities on various markers of semen quality.
Design: Crossover study.
Setting: Medical school.
Patient(s): Forty-five men participated voluntarily in the study, being allocated into three groups according to their
sports practice.
Intervention(s): None.
Main Outcome Measure(s): Sperm parameters (volume, liquefaction time, pH, viscosity, sperm count, motility,
and morphology).
Result(s): Sperm concentration; total sperm number; type ‘‘a,’’ ‘‘b,’’ and ‘‘d’’ velocity; and morphology were sig-
nificantly different among the practitioners of the three different training modalities. Morphology was the param-
eter showing the greatest difference, even reaching clinical relevance for the triathlete group (4.7%, poor prognosis
pattern). In addition, these parameters tended to decrease as training requirements increased.
Conclusion(s): There are differences in the seminal profiles of individuals exercising in different modalities. The
differences are more marked as intensity and volume of exercise increase, especially for morphology. These vari-
ables ought to be carefully analyzed and taken into account when designing a training protocol, especially with
higher-level athletes, so that reproductive function is not compromised. (Fertil Steril
2008;-:-–-.2008
by American Society for Reproductive Medicine.)
Key Words: Male infertility, seminal profile, water polo, triathlon, physically active, training, sports
The last few decades have seen a rising demand for sports ac-
tivities. Physical exercise is promoted as a panacea for fitness,
health, stress reduction, and life quality improvement, a matter
of great importance in today’s society (1). Despite this in-
creased interest, not having an adequate knowledge of how to
perform these activities might, on occasion, lead to the appear-
ance of negative side effects (e.g., lesions, pathologies). For ex-
ample, a trend toward a decline in reproductive function has
been reported not only in women but also in men as expressed
by the analysis of the semen (2–5). A number of studies
reported on the relevance and effects of physical exercise on
reproductive function. This association has been assessed
mainly in women because of unequivocal symptoms such as de-
layed menarche, oligomenorrhea, and amenorrhea (6–8) espe-
cially in runners (9, 10), gymnasts (11), and ballet dancers (12).
Alterations in the reproductive function of male athletes have
also been reported (3, 13). Early investigations pointed to exer-
cise volume as the variable most affecting reproduction, thus hy-
pothesizing a volume threshold for reproductive disorders (14,
15). Other authors have suggested that exercise intensity is
equally deleterious to, or even more so than, volume on repro-
ductive function (16, 17). Other parameters inherent in any spe-
cific exercise modality can be harmful to the reproductive
system, such as bike saddles because of friction (18). We hypoth-
esized that the continued practice of different sports modalities,
because of their inherent characteristics (volume and/or training
intensity, different energy requirements), can result in differences
in the practitioners’ seminal profiles. Thus, it was the aim of the
present study to analyze the semen profiles of three male popu-
lations with different types and levels of physical activity.
MATERIALS AND METHODS
Subjects
The study was approved by the Institutional Review Board of
the University of C
ordoba, and informed consent was ob-
tained from all participants. Healthy white men volunteered
Received June 12, 2008; revised August 13, 2008; accepted September 3,
2008.
D.V. has nothing to disclose. M.E.D.S.-G. has nothing to disclose.
J.M.G.-M. has nothing to disclose. R.V.-L. has nothing to disclose.
R.J.S. has nothing to disclose. S.C.O. has nothing to disclose.
Presented in part at the 13th Annual Congress of the European Congress
of Sport Sciences, Estoril, Portugal, July 9–12, 2008.
Reprint requests: Diana Vaamonde, Ph.D., Morphological Sciences De-
partment, School of Medicine, Universidad de C
ordoba, Avda. Men
en-
dez Pidal s/n 14071, C
ordoba, Spain (FAX: 34-957452166; E-mail:
fivresearch@yahoo.com).
0015-0282/08/$34.00 Fertility and Sterility
Vol. -, No. -,-2008 1
doi:10.1016/j.fertnstert.2008.09.010 Copyright ª2008 American Society for Reproductive Medicine, Published by Elsevier Inc.
ARTICLE IN PRESS
to participate in the study. A physician reviewed their medical
histories, ruling out possible reproductive alterations or
childhood illnesses that could interfere with semen produc-
tion (e.g., mumps, measles, varicocele, trauma to the genital
area). The volunteers had no previous known infertility or hy-
pothalamic-pituitary problems, although in most cases they
had not fathered children. Exclusion criteria included, there-
fore, surgery or conditions that could impair reproduction,
varicocele, and use of steroid hormones. Other factors that
could interfere with the semen parameters were evaluated;
such factors included diet, coffee, cigarette smoking, and al-
cohol consumption (evaluated through a 7-day qualitative
and quantitative questionnaire), as well as possible occupa-
tional activities thought to exert a negative impact on semen
quality, such as exposure to pesticides or paints or sitting for
long hours in transportation means.
The inclusion criteria were related to exercise and to repro-
ductive health, expressed as the following: not having any of
the aforementioned exclusion criteria, practicing a minimum
of 3 h/wk, and having a maximum oxygen uptake of at least
40 mL/min per kilogram. A total of 45 subjects participated
in the study. According to their own practice and training
characteristics subjects were allocated to one of the following
three groups: physically active subjects, water polo players,
and triathletes (Fig. 1).
The first group was composed of physically active subjects
(n ¼16) who did not practice any systematic resistance and
power training but exercised three times a week, for 1 hour
each session. The subjects in this group practiced several
sports (basketball, soccer, tennis, paddle ball) and partici-
pated in local university competitions (nonprofessional).
The second group was composed of water polo players
(n ¼14). The subjects in this group were champions of the
‘‘provincial’’ league for the 2004 to 2005 season and had
a more demanding training load, performing a total of five
training sessions a week with 90 minutes duration each.
The third group was composed of triathletes (n ¼15). The
subjects in this group were elite triathletes and participated
in the ‘‘Ironman’’ competition. Their total weekly training
volume was distributed as follows for each of the three disci-
plines (running [49.4 7.4 km], cycling [330.8 56.0 km],
and swimming [11.3 3.0 km]). The Ironman competition
included 3.8 km of swimming, 180 km of biking, and 42.2
km of running. The characteristics of the subjects with regard
to their backgrounds and morphofunctional and training
status are given in Table 1.
FIGURE 1
Flow diagram of participants. PA ¼physically active
subjects; WP ¼water polo players; TA ¼triathletes.
Vaamonde. Semen parameters and exercise. Fertil Steril 2008.
TABLE 1
Subjects’ demographics.
Physically Active Water Polo Triathletes
Subjects 16 14 15
Age (years) 19.0 1.8
a,b
25.5 3.2
b,c
33.1 3.5
a,c
Weight (kg) 73.1 8.3
a
79.9 10.7
b,c
74.5 7.6
a
Height (cm) 175.9 4.2
a
180.1 5.2
b,c
175.3 3.7
a
Body fat (%) 15.6 3.0
a,b
13.2 3.5
b,c
7.0 2.9
a,c
VO2max (ml/min/kg) 45.2 4.2
a,b
54.2 4.9
b,c
64.0 5.1
a,c
Years of training 1.6 0.7
a,b
4.0 1.1
b,c
8.1 3.2
a,c
Number of sessions/Week 3.3 0.4
a,b
5.0 0.0
b,c
9.9 1.8
a,c
Duration of session (min) 60.0 0.0
a,b
90.0 0.0
b,c
122.6 62.7
a,c,d
Sports category Local Regional International
Note: Values given as mean SD. Vo
2
max ¼maxmum oxygen uptake.
a
Significant differences (p<0.05) compared to water polo players
b
Significant differences (p<0.05) compared to triathletes
c
Significant differences (p<0.05) compared to physically active subjects
d
Mean of all sessions (cycling, swimming, running)
Vaamonde. Semen parameters and exercise. Fertil Steril 2008.
2Vaamonde et al. Semen parameters and exercise Vol. -, No. -,-2008
ARTICLE IN PRESS
Semen Analysis
The participants had a 3- to 6-day sexual abstinence period
preceding the semen sample collection and analysis. The tri-
athlete and water polo subjects were assessed 2 weeks after
the last competition and the last league match, respectively.
For semen analysis the subjects ejaculated into sterile urine
collection cups following the instructions given for the col-
lection and handling of the sample. On arrival at the labora-
tory, they completed a brief questionnaire indicating days
of abstinence and time of sample collection (arrival at the lab-
oratory was within a half hour of collection time) and noting
any sample collection problems. The macroscopic evaluation
was performed 30 minutes after sample collection, when
sample liquefaction was complete. In all cases complete liq-
uefaction occurred within the normal established time range.
The semen analysis included physical parameters (volume,
pH, liquefaction state, odor, color, absence or presence of ag-
glutination and gelatinous bodies, and viscosity), as well as
qualitative parameters of sperm (number, velocity, and mor-
phology). We examined the ejaculate volume (expressed in
milliliters), sperm concentration (expressed as million per
milliliter), velocity (classified as ‘‘a,’’ ‘‘b,’’ ‘‘c,’’ and ‘‘d’’
types), and morphology (expressed as percentage of normal
forms) as the standards for sample normality as the World
Health Organization recommends (19). Concentration and
motility were assessed with use of the Makler chamber
(Sefi Medical, Haifa, Israel). Sperm count was expressed as
million per milliliter (concentration) or total number in mil-
lions. Regarding velocity, sperm were classified as having ei-
ther type a, b, c, or d velocities. Type a were sperm that moved
at >20 mm/s; type b moved at a speed between 5 and 20 mm/s;
type c moved at <5mm/s, and type d were static. Two slides
of sperm smears were made for morphology assessment in
each case and stained with Diff-Quik stain (Dade Diagnos-
tics, Miami, FL). Morphology slides were observed at
1,000 with immersion oil analyzing 200 sperm per slide,
examining the head, midpiece, and tail with use of Kruger’s
strict criteria. In some cases, additional tests such as sperm
vitality or sperm antibodies were needed. Vital Screen (Ferti
Pro, Beernen, Belgium) was used for vitality testing, and
Sperm Mar Test (Ferti Pro) was used for antibody testing;
200 sperm were analyzed for each test.
Statistical Analysis
On the basis of a pilot study (six subjects), as well as available
literature, a power analysis was performed to determine the ap-
propriate number of subjects. Fourteen subjects were required
to detect a minimum difference of 25 million for total sperm
number, 15% in type a þb velocity, and 4% in morphology
(Granmo 5.2 for Windows; IMIM, Barcelona, Spain); this
would be required to achieve 80% statistical power.
Shapiro-Wilks tests were used to determine data normality
for all dependent variables. Series of one-way analysis of var-
iance (ANOVA) tests were used to compare groups for the de-
scriptive variables. This analysis revealed an age difference
between groups. Thus, analysis of covariance tests (ANCO-
VAs) were used with age as a covariance factor because of
its effect on seminal parameters. A Sidak correction was
used for multiple comparison purposes. Significance level
was set at P<.05 (SPSS 10.0 for Windows; SPSS Inc., Chi-
cago, IL).
RESULTS
All semen physical characteristics such as odor, color, and
time to liquefaction were normal in all cases, and no differ-
ences were observed among groups. The values obtained
TABLE 2
Semen parameters from the subjects from the three different exercise groups.
Mean (SD)
Physically Active Water Polo Triahtletes Pvalue
d
Volume (ml) 3.2 0.9 3.4 1.3 2.9 0.9 0.48
Sperm concentration (10
6
/mL) 61.0 23.0
b
58.0 24.4
b
48.2 14.7
a,c
0.04
Total sperm number (10
6
) 191.8 73.4
b
196.6 85.4
b
141.3 58.0
a,c
0.03
% Type ‘‘a’’ velocity 31.1 9.7
a
23.6 8.8
b,c
31.4 8.7
a
0.03
% Type ‘‘b’’ velocity 25.6 9.1
b
28.8 12.3
b
18.9 7.6
a,c
0.02
% Type ‘‘aþb’’ velocity 56.7 6.5 52.5 11.1 50.3 8.9 0.34
% Type ‘‘c’’ velocity 10.4 5.0 14.3 6.6 11.9 6.3 0.41
% Type ‘‘d’’ velocity 33.0 7.1
b
33.3 11.3 38.4 7.2
c
0.03
% Normal forms 15.2 1.2
a,b
9.7 3.0
b,c
4.7 2.2
a,c
0.01
a
Significant differences (p<0.05) compared to water polo players
b
Significant differences (p<0.05) compared to triathletes
c
Significant differences (p<0.05) compared to physically active subjects
d
One-way ANOVA and Sidak post hoc test for multiple comparisons
Vaamonde. Semen parameters and exercise. Fertil Steril 2008.
Fertility and Sterility
3
ARTICLE IN PRESS
for all the seminal parameters are shown in Table 2. It can be
noted that the values for all parameters showed a trend toward
higher values in the physically active group and lower for the
water polo and triathlete groups, reaching statistical signifi-
cance and, in some cases, even clinical significance as in
the case of morphology. Thus, the sperm concentration was
highest in the physically active group (61.0 10
6
/mL) fol-
lowed by water polo (58.0 10
6
/mL) and then triathlete
groups (48.2 10
6
/mL); ejaculate volume was similar for
the water polo and physically active groups whereas it was
lower for the triathletes. On the other hand, the total sperm
number was highest in water polo players and physically ac-
tive subjects and lowest in triathletes. With regard to sperm
velocity, the physically active group showed higher values
for type a þb velocity and lower values for type d velocity
(Table 2). Sperm morphology results were the most notewor-
thy, with statistical and clinical relevant differences among
the three groups (15.2% vs. 9.7% and 4.7% for physically ac-
tive, water polo, and triathlete, respectively). The difference
was statistically significant at P<0.001. It has to be noted
that the percentage of normal forms for water polo and triath-
lete groups was below the limits of normality for Kruger’s
strict criteria.
DISCUSSION
The main finding of this study was that sperm morphology
was significantly different among practitioners of the three
analyzed groups. Other parameters such as sperm concentra-
tion, total sperm number, and sperm velocity showed a similar
trend, albeit not as marked. Physical and macroscopic param-
eters were similar for the three groups and always in the range
of normality. To the best of our knowledge this is the first
study that analyzed differences in semen profiles of three
groups of healthy individuals practicing different sport
modalities.
Although sperm concentration was higher for the physi-
cally active group, total sperm number, a function of both
concentration and ejaculate volume, was slightly higher in
the water polo group. To the best of our knowledge, this is
the first study to report data on water polo players. Previous
studies have investigated mainly subjects who practice en-
durance sports. Ayers et al. (13) have observed that 10% of
a sample of marathon runners exhibited severe oligospermia.
We observed oligospermia in three of the triathlon subjects,
although it was not severe (range of 1.3–1.8 mL).
The physically active group showed a trend for higher
values of type a þb velocity forms (not significant). Despite
the fact that type a in water polo players and type b in triath-
letes were below 25%, all groups reached 50% in a þb,
thereby suggesting no impairment of motility. Our findings
seem to agree with those reported by other authors reflecting
a higher value for seminal parameters in control subjects as
compared with high-load exercise groups (2, 3, 14, 20);
among those reports, only Arce et al. (14) found statistical
differences. Statistically significant differences also were re-
ported by our group when comparing physically active sub-
jects who underwent high-intensity exercise with those who
kept their regular routines (17).
The last seminal parameter to be analyzed was morphol-
ogy. This structural test is gaining greater importance as a fac-
tor to be evaluated in human fertility analysis. Recent studies
have correlated morphology with the outcome of assisted re-
production techniques (21–26), as well as with in vivo con-
ception outcomes (22, 24). We have evaluated sperm
according to Kruger’s strict criteria (27, 28). Only the phys-
ically active group was above the 14% threshold value of
Kruger’s criteria (15.2%, N-pattern) in contrast to the water
polo group (9.7%, G-pattern) and the triathlete group
(4.7%, P-pattern). These differences reached not only statis-
tical significance but also clinical relevance in the case of tri-
athletes, because individuals with <5% normal forms are
considered subfertile (29). One might speculate that differ-
ences in sperm morphology might be due to age differences
observed between the groups; however, ANCOVA was
used, and the test showed no effect of age on the analyzed pa-
rameter. Moreover, according to Chen et al. (30) the expected
change in morphology would be a decrease of 1.06% per de-
cade. Certainly, the differences observed for water polo
players and triathletes are above that expected change.
Two factors that were not exercise related, water disinfec-
tion byproducts and water temperature, were excluded as
possible causes of the observed alterations. The swimming
pool where water polo players trained was treated via the
method of saline chlorination, which greatly reduces a poten-
tial toxicity variable, because it provides more stable and
reliable control of chlorine concentration. On the other
hand, the pool temperature is normally kept at approximately
27C. Thus, it is likely that the differences observed in water
polo players are due to inherent characteristics of their
training.
We found significant differences in several parameters,
with morphology being clearly the most altered; the triath-
letes showed a trend toward poorer seminal parameter values
than the other two groups, and they are the only ones who per-
form very high training volume (running: 49.4 km; swim-
ming: 11.3 km; cycling: 330.8 km). Arce et al. (14) report
that the athletes who exhibit differences in semen parameters
are those with a minimum running volume of 100 km/wk.
The triathletes analyzed in the present study did not have
that running volume, but after adding the swimming and
biking kilometers they surpassed it. It is difficult to find out
which of the modalities they practice can affect sperm the
most. Our study disagrees with the only other study that
analyzed triathletes, because that study reported no signifi-
cant differences in any of the seminal parameters (31);how-
ever, in measuring morphologic characteristics, those authors
did not use strict criteria and analyzed the three sperm
segments separately; perhaps differences could have been
found if they had used more standardized morphologic anal-
ysis. There are studies analyzing biking (5, 31), running (2, 3,
13, 14), and swimming (32–34) that demonstrate differences
4Vaamonde et al. Semen parameters and exercise Vol. -, No. -,-2008
ARTICLE IN PRESS
in hormonal and semen parameters. Investigating cycling,
Gebreegziabher et al. (5) reported only alterations in sperm
morphology. Despite following World Health Organization
regulations instead of Kruger’s strict criteria, they found dif-
ferences to be significant. Other authors reported diminished
sperm velocity but only during the competition period (31).
The subjects analyzed in the present study had been training
for a long time and showed significant alterations for some
parameters when compared with the physically active group.
We must point out, however, that our subjects were in a train-
ing phase in which the load had been reduced considerably,
because the evaluation was performed 2 weeks after they
had participated in the Ironman competition; therefore, we
may postulate that, as in the study by Lucia et al. (31), the
values for the parameters could have been lower during com-
petition or that because of the recent competition there still
could be a residual effect on the parameters.
We have not assessed hormonal profiles in this study, which
is a limitation; however, having analyzed the hormonal profile
would have contributed only a limited insight because many
times semen alterations occur without an associated hormonal
abnormality. In fact, researchers still question whether hor-
mone levels of FSH, LH, inhibin B, T, and thyroid hormones
really have a predictive value on semen quality because the
physiologic regulatory loops are rather complex and can be
confounding (35). Moreover, sperm production is a rather
long process requiring constant maintenance of testicular ho-
meostasis; thus, although hormonal values can be altered and
return to normal values, semen might not be able to revert to its
normal physiologic state as readily.
Only five studies analyzed the effects of swimming on re-
productive parameters; two exclusively assessed hormones in
elite swimmers (observing contradictory results), and the
other three analyzed reproductive capacity in rats. In rats sub-
mitted to heavy swimming, histologic sections through sem-
iniferous tubules showed a decrease in spermatid number,
which could be hazardous for reproductive health (34). More-
over, Manna et al. (36, 37) observed a decrease in several cell
lineages, as well as enzymes related to sex hormones and an-
tioxidant systems. Similar effects might be seen in humans if
the stress due to exercise were high enough. In fact, it has
been shown recently that the production of reactive oxygen
species during moderate exercise provokes an increase in
the expression of antioxidant enzymes, and, therefore, could
be considered an antioxidant itself. On the contrary, all ben-
efit is lost in exhaustive practice, possibly leading to oxida-
tive damage and cell damage (38). In addition, it seems
possible that the response might be dependant on the modal-
ity practiced (39–41). Moreover, Ironman triathletes have
been shown to exhibit oxidative damage as a result of training
and competition (39). We have mentioned the minimum run-
ning volume threshold (3, 15); however, as we have men-
tioned already, volume is not the only training parameter to
consider relative to reproductive function. All influential pa-
rameters must be studied carefully in the training context, and
an increase in scrotal temperature and reactive oxygen spe-
cies production, which are well known to adversely influence
seminal plasma and spermatozoa, should be avoided or min-
imized.
In conclusion, we observed that those practitioners system-
atically undergoing high training loads had altered values for
semen parameters. Thus, we consider that although perfor-
mance in these modalities needs such loads, palliative and
compensatory aspects ought to be taken in consideration to
dampen the effect of high-performance training. On the other
hand, we observed that practicing a less demanding physical
activity regularly does not seem to alter the values of normal-
ity of these parameters.
REFERENCES
1. Biolo G, Ciocchi B, Stulle M, Piccoli A, Lorenzon S, Dal Mas V, et al.
Metabolic consequences of physical inactivity. J Ren Nutr 2005;15(1):
49–53.
2. Griffith RO, Dressendorfer RH, Fullbright CD, Wade CE. Testicular
function during exhaustive endurance training. Phys Sportsmed
1990;18(5):54–64.
3. De Souza MJ, Arce JC, Pescatello LS, Scherzer HS, Luciano AA. Go-
nadal hormones and semen quality in male runners. A volume threshold
effect of endurance training. Int J Sports Med 1994;15:383–91.
4. Di Luigi L, Gentile V, Pigozzi F, Parisi A, Giannetti D, Romanelli F.
Physical activity as a possible aggravating factor for athletes with varico-
cele: impact on the semen profile. Hum Reprod 2001;16:1180–4.
5. Gebreegziabher Y, Marcos E, McKinon W, Rogers G. Sperm character-
istics of endurance trained subjects. Int J Sports Med 2004;25:247–51.
6. De Souza MJ, Metzger DA. Reproductive dysfunction in amenorrheic
athletes and anorexic patients: a review. Med Sci Sports Exerc
1991;23:995–1007.
7. Kopp-Woodroffe SA, Manore MM, Dueck CA, Skinner JS, Matt KS. En-
ergy and nutrient status of amenorrheic athletes participating in a diet and
exercise training intervention program. Int J Sport Nutr 1999;9:70–88.
8. De Souza MJ, Leidy HJ, O’Donnell E, Lasley B, Williams NI. Fasting
ghrelin levels in physically active women: relationship with menstrual
disturbances and metabolic hormones. J Clin Endocrinol Metab
2004;89:3536–42.
9. De Souza MJ, Luciano AA, Arce JC, Demers LM, Loucks AB. Clinical
tests explain blunted cortisol responsiveness but not mild hypercortiso-
lism in amenorrheic runners. J Appl Physiol 1994;76:1302–9.
10. Prather H, Hunt D. Issues unique to the female runner. Phys Med Rehabil
Clin N Am 2005;16:691–709.
11. Klentrou P, Plyley M. Onset of puberty, menstrual frequency, and body
fat in elite rhythmic gymnasts compared with normal controls. Br J
Sports Med 2003;37:490–4.
12. Valentino R, Savastano S, Tommaselli AP, D’Amore G, Dorato M,
Lombardi G. The influence of intense ballet training on trabecular
bone mass, hormone status, and gonadotropin structure in young women.
Clin Endocrinol Metab 2001;86:4674–8.
13. Ayers JWT, Komesu V, Romani T, Ansbacher R. Anthropomorphic, hor-
mone, and psychologic correlates of semen quality in endurance-trained
male athletes. Fertil Steril 1985;43:917–21.
14. Arce JC, De Souza MJ, Pescatello LS, Luciano AA. Subclinical alterations
in hormone and semen profile in athletes. Fertil Steril 1993;59:398–404.
15. De Souza MJ, Miller BE. The effect of endurance training on reproduc-
tive function in male runners. A ‘‘volume threshold’’ hypothesis. Sports
Med 1997;23:357–73.
16. Jensen CE, Wiswedel K, McLoughlin J, van der Spuy Z. Prospective
study of hormonal and semen profiles in marathon runners. Fertil Steril
1995;64:1189–96.
17. Vaamonde D, Da Silva ME, Poblador MS, Lancho JL. Reproductive pro-
file of physically active men after exhaustive endurance exercise. Int J
Sports Med 2006;27:680–9.
Fertility and Sterility
5
ARTICLE IN PRESS
18. Brock G. Erectile function of bike patrol officers. J Androl 2002;23:
758–9.
19. World Health Organization. Laboratory manual for examination of hu-
man semen and sperm-cervical mucus interaction. 4th ed. New York:
Cambridge University Press, 1999.
20. Bagatell CJ, Bremner WJ. Sperm counts and reproductive hormones in
male marathoners and lean controls. Fertil Steril 1990;53:688–92.
21. Kruger TF, Swanson RJ, Hamilton M, Simmons KF, Acosta AA,
Matta JF, et al. Abnormal sperm morphology and other semen parame-
ters related to the outcome of the hamster oocyte human sperm penetra-
tion assay. Int J Androl 1988;11:107–13.
22. Ombelet W, Menkveld R, Kruger TF, Steeno O. Sperm morphology as-
sessment: historical review in relation to fertility. Hum Reprod Update
1995;1:543–57.
23. Burr RW, Siegberg R, Flaherty SP, Wang XJ, Matthews CD. The influ-
ence of sperm morphology and the number of motile sperm inseminated
on the outcome of intrauterine insemination combined with mild ovarian
stimulation. Fertil Steril 1996;65:127–32.
24. Ombelet W, Bosmans E, Janssen M, Cox A, Vlasselaer J, Gyselaers W, et al.
Semenparameters ina fertileversus subfertile population:a need for change
in the interpretation of semen testing. Hum Reprod 1997;12:987–93.
25. Kruger TF, Coetzee K. The role of sperm morphology in assisted repro-
duction. Hum Reprod Update 1999;5:172–8.
26. Van Waart J, Kruger TF, Lombard CJ, Ombelet W. Predictive value of
normal sperm morphology in intrauterine insemination (IUI): a struc-
tured literature review. Hum Reprod Update 2001;7:495–500.
27. Menkveld R, Kruger TF. Advantages of strict (Tygerberg) criteria for
evaluation of sperm morphology. Int J Androl 1995;18(Suppl 2):36–42.
28. Franken DR, Smith M, Menkveld R, Kruger TF, Sekadde-Kigondu C,
Mbizvo M, et al. The development of a continuous quality control pro-
gramme for strict sperm morphology among sub-Saharan African labo-
ratories. Hum Reprod 2000;15:667–71.
29. Siebert T, van der Merwe H, Kruger T, Ombelet W. How do we define
male subfertility and what is the prevalence in the general population?.
In: Oehninger S, Kruger T, eds. Male infertility: diagnosis andtreatment.
London: Informa Healthcare, 2007:269–76.
30. Chen Z, Toth T, Godfrey-Bailey L, Mercedat N, Schiff I, Hauser R. Sea-
sonal variation and age-related changes in human semen parameters.
J Androl 2003;24:226–31.
31. Lucia A, Chicharro JL, Perez M, Serratosa L, Bandres F, Legido JC.
Reproductive function in male endurance athletes: sperm analysis and
hormonal profile. J Appl Physiol 1996;81:2627–36.
32. Bonifazi M, Bela E, Carli G, Lodi L, Martelli G, Zhu B, et al. Influence of
training on the response of androgen plasma concentrations to exercise in
swimmers. Eur J Appl Physiol Occup Physiol 1995;70:109–14.
33. Mackinnon LT, Hooper SL, Jones S, Gordon RD, Bachmann AW. Hor-
monal, immunological, and hematological responses to intensified train-
ing in elite swimmers. Med Sci Sports Exerc 1997;29:1637–45.
34. Mingoti GZ, Pereira RN, Monteiro CM. Fertility of male adult rats sub-
mitted to forced swimming stress. Braz J Med Biol Res 2003;36:677–81.
35. Meeker JD, Godfrey-Bailey L, Hauser R. Relationships between serum
hormone levels and semen quality among men from an infertility clinic.
J Androl 2007;28:397–406.
36. Manna I, Jana K, Samanta PK. Intensive swimming exercise–induced
oxidative stress and reproductive dysfunction in male wistar rats: protec-
tive role of alpha-tocopherol succinate. Can J Appl Physiol 2004;29:
172–85.
37. Manna I, Jana K, Samanta PK. Effect of different intensities of swim-
ming exercise on testicular oxidative stress and reproductive dysfunction
in mature male albino Wistar rats. Indian J Exp Biol 2004;42:816–22.
38. Gomez-Cabrera MC, Domenech E, Vi~
na J. Moderate exercise is an anti-
oxidant: upregulation of antioxidant genes by training. Free Radic Biol
Med 2008;44:126–31.
39. Knez WL, Jenkins DG, Coombes JS. Oxidative stress in half and full
Ironman triathletes. Med Sci Sports Exerc 2007;39:283–8.
40. D
ek
any M, Nemesk
eri V, Gy€
ore I, Harbula I, Malomsoki J, Pucsok J. An-
tioxidant status of interval-trained athletes in various sports. Int J Sports
Med 2006;27:112–6.
41. Kostaropoulos IA, Nikolaidis MG, Jamurtas AZ, Ikonomou GV,
Makrygiannis V, Papadopoulos G, et al. Comparison of the blood redox
status between long-distance and short-distance runners. Physiol Res
2006;55:611–41.
6Vaamonde et al. Semen parameters and exercise Vol. -, No. -,-2008
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