Vol. 11, No.

2 83

ORIGINAL RESEARCH

The impact of blood and seminal plasma zinc

and copper concentrations on spermogram and
hormonal changes in infertile Nigerian men
Oluyemi Akinloye 1,2, Fayeofori M. Abbiyesuku3, Oluwafemi O.
Oguntibeju2, Ayodele O. Arowojolu4, Ernie J. Truter2
2
Oxidative Stress Research Centre, Department of Biomedical
Sciences, Faculty of Health and Wellness Sciences, Cape Peninsula
University of Technology, Bellville, South Africa; 3Department of
Chemical Pathology, 4Department of Obstetrics and Gynaecology,
College of Medicine, University of Ibadan, Nigeria

Received: 20 May 2010; accepted: 5 April 2011

SUMMARY
Zinc (Zn) and copper (Cu) concentrations in sera and seminal plasma
of 60 infertile males (40 oligozoospermic and 20 azoospermic) and 40
males with evidence of fertility (normozoospermic; controls) were
estimated using atomic absorption spectrophotometry. The results
were correlated with the subject’s spermogram and hormonal levels in
order to determine their relationship and significance in male
infertility. The mean serum concentration of zinc was significantly
(p<0.01) higher in oligozoospermic males when compared to
azoospermic subjects and controls. The ratios of serum Zn to seminal
plasma Zn were 1:1, 1:3 or 1:4 in oligozoospermic, normozoospermic
or azoospermic subjects, respectively. While the mean Cu
concentration was significantly higher in serum than seminal plasma
in all groups, the Zn concentration was significantly (p<0.05) higher
in seminal plasma than serum. The Cu/Zn ratio in seminal plasma was

1
Corresponding Author: Department of Biomedical Sciences, Faculty of
Health and Wellness Sciences, Cape Peninsula University of Technology,
Bellville 7535, South Africa; e-mail: Oluyemiakinloye@hotmail.com
84 Akinloye et al

significantly (p<0.01) higher in controls compared with other groups.

A significant (p<0.01) inverse correlation was observed between
serum Zn and sperm counts. Similarly, seminal plasma Zn negatively
correlated with spermatozoa viability. In conclusion, the measurement
of serum Zn level, apart from being a good index of the assessment of
prostatic secretion and function, may be considered a useful tool in
addition to other parameters in assessing male infertility. Also, a lower
Cu/Zn ratio in seminal plasma may serve as a supportive tools in
assessing male infertility. Reproductive Biology 2011 2: 83-98.
Key words: serum, seminal plasma, zinc, copper, male infertility,
hormones, spermogram

INTRODUCTION
Several trace elements have been shown to be essential for testicular
development and spermatogenesis [11, 27]. Bertrand and Vladesco [8]
first noticed the presence of zinc (Zn) in semen, which later was found
to be secreted into the seminal plasma by the prostate [13, 21].
Similarly, it has been reported that the majority of copper (Cu) present
in seminal plasma originates from the prostate. However, unlike Zn,
copper is also released by other structures of the reproductive tract
(e.g. epididymis, seminal vesicles; [34]). Seminal plasma serves as a
vehicle for spermatozoa transportation to the vagina.
Seminal plasma changes in trace element levels were related to the
fertilizing capacity of spermatozoa [25]. In human semen, Zn plays an
important role in spermatozoa physiology. Therefore, its deficiency
has been implicated in gonadal dysfunction, a decreased testicular
weight and shrinkage of the seminiferous tubules [7, 27].
Asthenozoospermia has been associated with low serum Cu
concentration, and Cu/Zn was higher in asthenozoospermic, infertile
males than in fertile males [38]. A few studies reported the possible
relationship between Cu, Zn and infertility [13, 37, 38]. These reports
varied in respect to concentrations of these elements in semen plasma
as well as their role in male infertility. This study was designed to
investigate relationships between: 1/ serum and seminal plasma
concentrations of Zn or Cu, 2/ serum or seminal plasma
concentrations of Zn or Cu and selected biophysical semen
parameters, and 3/ serum or seminal plasma concentrations of Zn or
Cu and testosterone or gonadotropin serum or seminal plasma
concentrations in infertile Nigerian men.
 Zinc and copper in male infertility 85

MATERIALS AND METHODS

Subjects
All voluntary males of infertile couples recruited into the study
attended infertility clinics at University College Hospital in Ibadan,
Nigeria and conformed to the specific selection criteria. The study
design included three male groups (age: 20–55 years) based on sperm
count: males with a sperm count less than 20 million/ml
(oligozoospermia; n=40; mean agerSEM: 35r1.2); males with no
spermatozoa in semen (azoospermia; n=20; mean agerSEM:
35.2r1.0); and healthy fertile control males with a sperm count greater
than 20 million/ml (normozoospermia; n=40; mean agerSEM:
36.6r1.0). Exclusion criteria were as follows: testicular varicocele,
genital infections (e.g. urethritis, prostatitis, sexually transmitted
diseases), chronic illness and serious systemic diseases (e.g. diabetes,
endocrine and metabolic disorders), heavy smoking and chronic
alcohol intake and previous groin or scrotal surgery. Moreover, male
contraceptives users (e.g. condoms, spermicides), men taking
medications for a long-term (e.g. antihypertensive drugs) and known
human immunodeficiency virus (HIV)-positive patients were excluded
from the study. The clinical evaluation and response to questionnaires
were used as the bases for subject selection. The control subjects were
recruited mainly from semen donors for intrauterine fertilization and
male partners of pregnant women and nursing mothers attending the
Antenatal Clinic of the Department of Obstetrics and Gynaecology,
University College Hospital in Ibadan. The control subjects were
recruited from a similar population, having similar demographic
characteristics. A normal semen analysis with a sperm count >20
million/ml (normozospermia) and having at least two living children
were used as criteria for selecting the control subject in addition to the
exclusion criteria used in the selection of other groups. All subjects
were required to give their informed consent. Ethical approval was
granted by the ethical committee of the College of Medicine
University of Ibadan and University College Hospital Ibadan.
86 Akinloye et al

Biophysical analysis of semen samples

A semen sample was collected from each subject on two occasions,
two weeks apart, after at least three days but not more than six days of
abstinence. The sample was obtained by masturbation into a
prewarmed clean wide-mouth sterile container in a private room near
the laboratory. The biophysical semen parameters were assessed
according to the WHO standard manual method using the WHO
guidelines for the examination of human semen and semen–cervical
mucus interactions [36]. The microscopic examination of semen
samples (sperm counts, percentage of spermatozoa with normal
morphology, sperm viability and motility, mean progressive motility)
was done at room temperature with light microscope (Olympus,
Germany). A supravital staining technique using eosin was used for
viability assay, while Giemsa stain was used for morphological
examination. The mean progressive motility (MPM) graded by WHO
(A-D) was modified (1-4) for statistical convenience. All reagents
were of analytical grade and were purchased from British Drug
Houses (Poole, UK) unless stated otherwise.

Hormonal assays
About 10 ml of venous blood was collected from the antecubital vein
of each subject into plain tubes between 9:00 and 10:30 AM. After
clot retraction, the sample was centrifuged at 3000×g for 5 min. The
serum was collected and stored at –20°C until analyzed. After the
analysis of spermogram, the semen samples were also centrifuged at
3000×g, and supernatant (seminal plasma) was collected and stored at
–20°C until further analysis. Serum and seminal plasma LH, FSH,
prolactin (PRL) and testosterone (T) assays were carried out using an
enzyme immunoassay (EIA) developed for the special research
program in human reproduction by WHO [35]. The samples were
assayed in duplicates with acceptable values with internal variation of
less than 15%. FSH minimum detectable dose (sensitivity limit) was
0.2 IU/l, LH: 0.1 IU/l, PRL: 2.0 nmol/l and T: 0.4 nmol/l.

Determination of trace elements

Concentrations of Zn and Cu in serum and seminal plasma samples
were determined by atomic absorption spectrophotometry using a
Buck Model 210-VGI (Bulls Scientific, East Norwalk, CT)
spectrophotometer at wavelength of 214 nm for zinc and 247 nm for
 Zinc and copper in male infertility 87

copper with a detection limit of 0.005 ppm for both elements. The
serum and seminal plasma metals were first released from the protein
matrix by the nitric and hydrochloric acid (1:1) wet digestion method
[15]. The samples’ elements were determined by direct aspiration of
the acidic sample into the atomic absorption spectrophotometer (AAS)
flame [28]. This complies with the specification for standardized
flame AAS quick procedure for metals when using the Buck Model
201 atomic absorption system. Similarly, the determination of
selenium (Se) and cadmium (Cd) in serum and seminal plasma of the
subjects was described previously [3, 5] with a wavelength of 196 nm
for Se and 226 nm for Cd, and detection limit of 0.15 ppm and 0.01
ppm, respectively.

Statistical analysis
The Statistical Package of Science and Social Sciences Version 15.0
(SPSS Inc.; Chicago, IL, US) software was used in statistical analysis.
Sperm biophysical characteristics were log transformed. The results
were expressed as mean±SEM. Significant differences among the
three examined groups were analyzed first by one-way ANOVA
followed by an LSD test. Significant differences between two
variables were determined by student t test. The relationships between
the examined parameters were measured with Pearson’s correlation.

RESULTS
The admission characteristics of each group of subjects were similar to
those described in our previous papers [4, 5]. The sperm biophysical
parameters of the infertile subjects were found to be significantly lower
than those of the controls, except for semen volume which was similar in
all groups. The normozoospermic group has a mean semen volume of
2.43±0.32 ml, sperm count of 72.7±5.89 million, viability of 80.5±1.35%,
percentage of normal spermatozoa 84.5±1.14%, motility 79.52±1.82% and
mean progressive motility 3.4±0.11. The oligozoospermic subjects have a
mean semen volume of 2.51±0.32 ml, sperm count 5.46±1.14 million,
viability 46.8±5.01%, percentage of normal spermatozoa 55±5.76%,
motility 35.75±4.95% and mean progressive motility 1.8±0.21.
Azoospermic males have a mean semen volume of 2.89±0.77 ml. In
addition, these males had no spermatozoa. Except for T levels, there were
no significant differences in seminal plasma hormone levels among the
three groups. Serum T was lower in normozoospermic subjects as
88 Akinloye et al

compared to oligo- and azoospermics. The mean serum T level was

5.92±0.59 nmol/l in the normozoospermic group, 6.70±3.06 nmol/l in the
oligozoospermic group, and 20.27±16.27 nmol/l in the azoospermic group,
while seminal plasma T levels were 4.02±0.57 nmol/l, 14.62±2.39 nmol/l
and 14.63±2.07 nmol/l, respectively. The T level was significantly
(p<0.05) higher in the infertile subjects than in the controls. This increase
was more pronounced in the azoospermic than oligoozospermic subjects.
Serum zinc concentration was significantly (p<0.001) higher in the
oligozoospermic group as compared to those of the control and
azoospermic groups (tab. 1). No significant (p>0.05) difference between
the control and azoospermic subjects was observed. Copper concentration
did not differ among the groups (p>0.05). There was also no significant
(p>0.05) difference in the seminal plasma levels of either element among
the groups. In general, the seminal plasma zinc levels were found to be
significantly (p<0.001) higher than those of serum. In addition, the
oligozoospermic subjects showed a Zn serum/seminal plasma ratio of 1:1
which was significantly different from normozoospermic (1:3) and
azoospermic subjects (1:4). The serum Cu level was significantly
(p<0.001) higher in all groups as compared to seminal plasma, with no
differences in the serum/seminal ratio among groups. The Cu/Zn ratio was
significantly higher in the serum than seminal plasma in all groups. The
ratio of Cu/Zn in the serum was significantly (p<0.01) lower in the
oligozoospermic group compared to the normozoospermic and
azoospermic males. The seminal plasma Cu/Zn ratio was shown to be
significantly (p<0.01) higher in the normozoospermic males compared to
the infertile subjects.
The serum zinc level showed a significant (p<0.01) inverse correlation
with sperm count and the seminal plasma Zn level demonstrated a similar
inverse correlation with sperm viability (p<0.05; tab. 2). Seminal plasma
Cu level was positively correlated with semen volume (p<0.05). Moreover,
the serum Zn level showed a significant (p<0.05; tab. 3) positive
correlation with the seminal plasma T level, while the seminal plasma Zn
level was positively correlated with serum LH (p<0.01) and FSH (p<0.01).
There was no significant correlation between Cu and hormone levels. In
addition, we observed a significant (p<0.05; tab. 4) positive correlation
between the serum Zn and Cu levels. Furthermore, these levels showed a
positive correlation with serum selenium (p<0.05). On the other hand, serum
Zn showed an inverse correlation with seminal plasma Se and cadmium levels
(p<0.001) and serum Cu with seminal plasma cadmium (p<0.01; tab. 4).
 Zinc and copper in male infertility 89

Table 1. Serum and seminal plasma of zinc and copper concentrations

(mean±SEM) in studied subjects

Significant differences among the three groups were analyzed by ANOVA followed
by LSD test, different superscripts depict within a row significant differences among
groups; *denote significant differences between serum and seminal plasma
concentrations of respective parameters, analyzed by Student t test.

Table 2. Correlation coefficients (r) between zinc or copper levels and

semen biophysical parameters

Values are expressed as r; absolute values of spermogram are available in our

previous publications [4, 5]. + positive correlation; – negative correlation;
*significant correlation p<0.05; MPM: mean progressive motility of sperm (unit:
absolute values).
90 Akinloye et al

Table 3. Correlation coefficients (r) between zinc or copper and

hormone levels in serum and seminal plasma

Values are expressed as r; absolute values of hormones are available in our previous
publications [4, 5]. + positive correlation; – negative correlation; *significant
correlation p<0.05; LH: luteinizing hormone; FSH: follicle stimulating hormone;
PRL: prolactin; T: testosterone

Table 4. Correlation coefficients (r) between serum and seminal

plasma concentrations of trace elements

+ positive correlation; – negative correlation; significant correlation: *p<0.05,

**p<0.01, ***p<0.001

DISCUSSION
This study is the first to report a possible contribution of serum and
seminal plasma Zn and Cu to infertility in Nigerian men. It had been
reported that Zn was high in adult testis [7] and the prostate had a
higher Zn concentration than any other organ of the body [19]. The
 Zinc and copper in male infertility 91

higher concentration of Zn in seminal plasma than in serum

demonstrated in our study is in accordance with most previous studies
[22, 27]. In contrast, Cu is released from all structures of the male
reproductive tract with prostate being its main source [34]. Thus, the
elements appear to be important for male reproduction. Zinc was
reported to be necessary for growth, sexual maturation and
reproduction [23] as well as in nucleic acid metabolism [16, 29].
A significant correlation between serum and seminal plasma Zn
levels was demonstrated previously [23]. Such relationship was not
observed in the current study. Furthermore, in accord with findings of
others [17, 25], we also did not observe a significant difference in the
seminal plasma Zn levels between our infertile subjects and controls.
However, we report for the first time significant differences in the Zn
serum-seminal plasma ratio among oligozoospermic (1:1),
normozoospermic (1:3) and azoospermic (1:4) subjects. This implies
that although the changes in the element concentrations may not have
a direct effect on spermatogenic failure, there may be an indirect
effect on reducing spermatogenesis. The difference in the Zn serum-
seminal plasma ratio was due to a significant high serum Zn level in
oligozoospermic subjects compared to the other groups. This indicates
that Zn toxicity may contribute to the poor semen quality in
oligozoospermic subjects.
Transient derailments in semen quality were reported as a result of
exposure to high levels of air pollution [31]. This phenomenon was
associated with acidic sulfates, organic compounds and toxic trace
elements [13]. However, more evidence has been reported on the
effects of Zn depletion on reproduction, with little interest or emphasis
on the possibility of its likely toxic effect. The 1:1 Zn serum:seminal
plasma ratio found in oligozoospermic subjects compared with the 1:3
ratio in normozoospermic patients is a possible indication of a
physiological deficiency of Zn in the male reproductive organs. Our
observation of a significant higher level of Zn in the seminal plasma
compared to that in serum is in line with data of other studies [22, 27,
36]. Sørensen et al. [30] also demonstrated that serum Zn is lower than
that of the prostate. This implies that the prostate concentrates Zn
from the blood and secretes precise quantities into seminal plasma.
The serum:seminal plasma Zn ratio observed in oligozoospemic
subjects (1:1) may imply the failure of the prostate to effectively
92 Akinloye et al

perform this role, leading to a physiological depletion in Zn and a

resultant accumulation of Zn in the serum.
A significant inverse correlation between serum Zn and sperm
counts observed in this study, which is inconsistent with some
previous findings [20, 27], but consistent with others [6, 24, 26],
further supports this hypothesis. Abou-skakra et al. [2] postulated that
the role of trace elements in infertility was more directly related to
their sperm and serum levels than to the seminal plasma level. The
negative correlation between seminal plasma Zn and sperm viability is
a good indication of the importance of Zn in spermatogenesis. This
may be explained by the essential role of Zn in protein metabolism
[14] and nucleic acid synthesis [33], i.e. in processes important in
spermatogenesis.
Copper is a normal constituent of semen bound to the tail
midpiece of spermatozoa [20] and present in seminal plasma, ampullar
and seminal vesicular fluids [10]. Valsa et al. [34] measured the
copper level in three splits of twenty one ejaculates to locate the origin
of Cu in semen. The Cu level was high in the first split and low in the
second one. This indicates that Cu is released from all parts of the
genital tract even though the major source is the prostate gland. Our
current data on Zn and Cu together with our previous results on Se
and Cd [3, 5] showed that in normozoospermia and azoospermia,
serum Zn level was the highest, and it was followed consecutively
by Cu, Cd and Se (Zn>Cu>Cd>Se). This pattern was altered
in oligozoospermia with serum Se being higher than Cd
(Zn>Cu>Se>Cd). This strengthens the notion that alterations in trace
element status contribute to the reduction of sperm quality.
Unlike Zn, the Cu level was significantly higher in serum than the
seminal plasma. As in other studies [17, 32] there was no significant
difference in seminal plasma Cu level among the three groups of
subjects. The values reported in this study were lower than those
reported by Stankovic et al. [32] and similar to those reported by
Ladipo et al. [17]. Apart from poor nutritional intake of Cu-rich food
as was adduced by these authors as the possible cause of this
difference, environmental variation is implicated.
The correlations which were found between Zn level (present
study) or Cd and Se levels (previous studies: [3, 5]) and spermograms
were not demonstrated for Cu and semen biophysical parameters. An
exception was a significant positive correlation between the seminal
 Zinc and copper in male infertility 93

plasma Cu level and semen volume. Also, Valsa et al. [34] concluded
that the Cu level did not correlate with the studied semen parameters.
The similar pattern in the serum-seminal plasma ratio in
normozoospermic (6:1), oligozoospermic (7:1) and azoospermic (5:1)
subjects is consistent with this conclusion. Therefore, it is not
surprising that seminal plasma Cu correlated positively with semen
volume, a parameter that is not different in the studied three groups.
The relative high serum testosterone and gonadotropins
concentrations and high seminal plasma testosterone found in infertile
subjects suggest a derangement in the mechanism for T uptake at the
cellular level in the pituitary or testes [4]. Hypergonadotropism and
hypergonadism in infertile males has been reported as an indication of
Sertoli cell failure [4]. The significant positive correlation between the
seminal plasma Zn and serum gonadotropin hormones (LH and FSH)
suggests that zinc may have a direct effect on the pituitary-gonadal-
axis. The increase in gonadotropins with resultant stimulation of
Leydig cells may be responsible for the high T level observed in our
infertile males. There is evidence that the supplementation of Zn
increased the serum T level in men and animals [9, 16,24] confirming
that a low Zn level is associated with hypogonadism [1, 11]. This may
be explained by the Zn role in activating the adenyl cyclase system,
which is involved in the stimulation of steroidogenesis [12]. Direct
stimulation of Leydig cells might enhance T production [16]. The
strong positive correlation between serum Zn and T levels supported
this claim. Although, we did not observe such an association between
the Cu level and hormones of the pituitary-gonadal-axis, the serum Cu
had a significant positive correlation with serum Zn. This implies that
Cu concentration may exert an indirect effect on the pituitary-gonadal-
axis and spermatogenesis.
We correlated our previously reported serum and seminal plasma
Se and Cd data with the data from the current study – both studies
were performed on the same population. We observed strong
relationships between the serum level of Zn or Cu and Se or seminal
plasma Cd. The serum Cu level was positively correlated with serum
Zn and Se and negatively correlated with seminal plasma Cd. We had
previously reported the importance of an optimum concentration of Se
in improving male fertility [3] and the toxic effect of Cd in infertile
males [5]. The inverse relationship between serum Zn or Cu with
seminal plasma Cd may underlie a physiological mechanism
94 Akinloye et al

preventing Cd toxicity, especially, in highly exposed populations like

Nigeria [5]. Dietary supplementation of these elements, particularly
Zn, may be an important intervention in the management of disorders
associated with Cd toxicity including male infertility. Likewise, a
strong relationship between serum/seminal plasma Zn/Cu levels and
serum Se observed in our study may be important in maintaining the
required optimum concentration of Se, an essential element for male
fertility [3]. Knowledge of the relationship and synergistic interaction
between trace elements are therefore very important in trace element
dietary supplementations.
In conclusion, the results of the current study implicate that a low
cellular zinc level is a contributing factor to reduced spermatogenesis
and low cellular testosterone in infertile Nigeria males. Copper
appears to play an indirect role in male infertility either by increasing
or reducing the bioavailability of other elements, which consequently,
may have a positive or negative influence on male fertility. Our
observations suggest that the Cu/Zn ratio may be a preferred tool for
the assessment of the involvement of low cellular Zn level in male
infertility. The observed interactions between Zn and other elements
call for the consideration of these trace element levels for
supplementation intervention.

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