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Original Studies |
Department of Growth and Reproduction (T.K.J., A.-M.A., A.G., N.E.S.), Rigshospitalet, DK-2100 Copenhagen, Denmark; Department of Occupational Medicine (N.H.I.H., H.K., J.P.B.), University of Aarhus; Department of Biostatistics (T.S.), University of Copenhagen; Department of Obstetrics and Gynaecology (T.B.H., E.E.), Aarhus University Hospital; The Danish Epidemiology Sciences Centre (J.O.), Aarhus University; Centre for Reproductive Biology (A.M.), Medical Research Council, Edinburgh; and School of Biological and Molecular Sciences (N.P.G.), Oxford Brookes University, Oxford
Address all correspondence and requests for reprints to: Tina Kold Jensen, Department of Growth and Reproduction, The National University Hospital, Rigshospitalet, sect. GR 5064, 9-Blegdamsvej, DK-2100 Copenhagen, Denmark.
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Abstract |
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 Top Abstract IntroductionSubject and MethodsResultsDiscussionReferences |
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From 1992 to 1995, a total of 430 men, 20–35 yr old, who lived with a partner and who had not previously attempted to achieve a pregnancy, were recruited. The couples were enrolled into the study in one of two centres (centre A, n = 231; and centre B, n = 199) when they discontinued birth control. At enrollment, they provided a semen sample (n = 419), and a blood sample was drawn (n = 349). The semen analysis was performed in accordance with the WHO 1992 guidelines, and interlaboratory differences were tested. Inhibin B was measured in an enzyme immunometric assay, which has previously been described. All blood samples were analyzed in the same laboratory.
Median sperm concentration and the percentage of morphologically normal spermatozoa were significantly higher among men from centre A (56.0 mill/mL and 42.5%), compared with men from centre B (44.8 mill/mL and 39%). Men from centre B had a significantly higher median FSH (3.42 IU/L) and a lower inhibin B (186 pg/mL) than men from centre A (3.21 IU/L and 209 pg/mL). The differences persisted after control for potentially confounding variables. A significant correlation was found between the cubic root-transformed serum FSH and inhibin B levels (r = -0.61, P < 0.001), between the cubic root-transformed serum FSH and sperm concentration (r = -0.40, P < 0.001), and between the cubic root-transformed inhibin B and sperm concentration (r = 0.38, P < 0.001). The predictive power of detecting sperm counts below 20 mill/mL among men who’s inhibin B and FSH both were below 80 pg/mL and above 10 IU/L, respectively, was 100%.
The unexpected significant difference in semen concentration between two groups of normal Danish men was probably caused by differences in sampling procedures in the two centres where the men were recruited, rather than geographical differences. However, similar differences in serum levels of inhibin B and FSH between centres were found. These findings suggest that a real difference in spermatogenic potential between the two groups of men existed. We suggest that serum inhibin B, in future population studies on male reproductive health, may serve as a new marker of spermatogenesis, in addition to sperm concentration and serum FSH.
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Introduction |
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TopAbstractIntroductionSubject and MethodsResultsDiscussionReferences |
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In a Danish, nationwide, collaborative study, we had the opportunity to investigate semen samples and reproductive hormones, including FSH and inhibin B, among 349 normal Danish men. The men were enrolled differently in two regions. Although the primary objective of the study was not to identify regional differences, we found a significant difference in sperm counts between the two populations. Given that serum inhibin B concentrations correlate with semen quality, it was of interest to see whether a parallel difference in inhibin B was present.
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Subject and Methods |
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TopAbstractIntroductionSubject and MethodsResultsDiscussionReferences |
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The aim of the original study was to describe the association between time to pregnancy and semen quality in a population with unknown fertility. Four nationwide unions (i.e. metal workers, trade and office workers, nurses, and day care workers) provided personal identification numbers of all members throughout the country. Members between 20–35 yr of age, cohabiting with a person of the opposite sex and in the same age range, with no children at the same address, were identified (n = 52,255). From August 1992 through September 1995, they were mailed a personal letter and invited to join the study. Inclusion criteria were: no previous pregnancies; no prior knowledge of fertility; living with a person of the opposite sex; current use of contraception but planning to discontinue within the study period to conceive. A total of 430 couples from all over Denmark participated. It was estimated that 10–20% of eligible couples participated (6). Because the couples lived in different parts of the country, they were enrolled in the study in two centres (centre A, n = 231; and centre B, n = 199). The protocol was approved by The National Ethical Committee.
At enrollment, both partners filled in a questionnaire on demographic, medical, reproductive, occupational, and lifestyle factors. The males provided a semen sample (n = 419) and a blood sample (n = 349). At centre A, the couples who lived far from the centre hospital were interviewed at their home address, because of the long distances, whereas all participants at centre B were interviewed at the centre hospital. Blood samples were collected from 162 men (82.7%) from centre B and 187 men (83.9%) from centre A. At centre B, a semen sample was collected at the home address among couples who achieved a pregnancy before the interview (n = 16). Therefore, no blood samples were drawn from these couples. All questions regarding diseases of the reproductive organs were analyzed, in relation to fecundability, and those found to affect fecundability (adult parotitis, testicular cancer, and cryptorchidism) were transformed into one variable: present or not present.
Semen and blood collection and analysis
Semen samples were obtained by masturbation only and were collected at the home residence. We encouraged sampling after 3 days of abstinence but emphasized that samples obtained outside this time window would still be useful. The ejaculates were collected directly into a 50-mL polyethylene container, and 93.8% were examined within the first 2 h (no difference between centres). Men from centre B poured the semen sample from a large to a smaller portable container at home, whereas this was done by a technician at centre A. The semen analysis was performed in accordance with the WHO 1992 guidelines (7). After complete liquefaction, the sample was kept in a heated chamber at 37 C until analysis. The semen volume was measured in a graded tube with 0.1 mL accuracy. Sperm concentration was measured in a Makler chamber at centre A and in a Bürger-Türk chamber at centre B. An appropriate dilution was determined after a preliminary examination of the undiluted sample. Counting was undertaken using a phase-contrast microscope at a magnification of 200. The sample was counted twice, and if there was more than 10% difference between the two counts, the sample dilution was remixed and the counting procedure was repeated. Morphological evaluation was performed only by one technician. The interlaboratory variation in sperm count was tested by comparing sperm counts on the same 28 samples made by a technician from each of the two centres, and no systematic difference was found (interlaboratory coefficient 0.96, paired t test = 0.23, P = 0.82).
Serum was separated after clotting and stored at -20 C until hormone
measurements. No differences between storage times existed between
centres. With regard to the different hormone assays, all serum samples
were analyzed in the same laboratory. Inhibin B was measured in an
enzyme immunometric assay, which has previously been described (4, 8).
The inhibin B assay, which is specific for the bioactive inhibin B
dimer (
-ßB), uses an immobilized monoclonal capture
antibody raised against a sequence from the human
ßB-subunit and a secondary enzyme-conjugated monoclonal
antibody raised against a sequence from the human -subunit. The
sensitivity of the inhibin B assay was 20 pg/mL, and the intra- and
interassay coefficients of variation were <12% and <17%,
respectively. Serum concentrations of FSH and LH were measured using
time-resolved immunofluorometric assays from Wallac, Turku, Finland.
The sensitivity of the FSH and LH assays was 0.06 IU/L and 0.05 IU/L,
respectively. In both assays the intra- and interassay coefficients of
variation were <10%. Serum testosterone was measured using an RIA
(Coat-a-Count) from Diagnostic Products Corporation, Los Angeles, CA).
The sensitivity of the Diagnostic Products Corporation testosterone
assay was 0.23 nmol/L, and the intra- and interassay coefficients of
variation were both <10%.
Statistical analysis
Frequency distributions of the various semen and blood parameters were highly skewed, and nonparametric tests were used to test differences in parameters between centres. Cubic root transformation showed good approximation to the normal distribution in the residual plots. Multiple linear regression analysis was done on the cubic root-transformed semen and blood parameters as dependent variables, and potentially confounding variables were included in the model. The potential confounding variables were excluded stepwise if they had no impact on the dependent variable.
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Results |
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TopAbstractIntroductionSubject and MethodsResultsDiscussionReferences |
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Table 1
shows the values for semen
parameters in the two groups of men. Sperm concentration, volume, total
sperm count, and the percentage of morphologically normal spermatozoa
were significantly higher among men from centre A, compared with men
from centre B. Men from centre B had a smaller seminal volume, which
was probably because of the fact that they poured the sample from one
container to another at home, which the men from centre A did not. This
may also explain the observed difference in total sperm count (sperm
concentration multiplied by seminal volume).
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). More men from centre B delivered their
semen sample in the winter, from September to March. The median time of
the day for blood sampling among men at centre B was 1030 h,
whereas it was 1430 h among men at centre A. The men from whom no
blood sample was drawn did not differ from the rest, with respect to
semen quality, age, weekly alcohol intake, percentage of smokers, or
percentage with diseases of the reproductive organs. Reproductive hormones
Significant correlations were found between serum FSH and inhibin
B levels [r = -0.44, P < 0.001 (nontransformed
parameters); or r = -0.61, P < 0.001 (cubic
root-transformed parameters), Fig. 1].
The correlations did not differ according to centres.
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and among men from the two centres. Similar associations were found
between serum inhibin B and sperm concentration [r = 0.26,
P < 0.001 (nontransformed parameters); or r =
0.38, P < 0.001 (cubic root-transformed parameters),
Fig. 3]. We performed all correlations
after exclusion of men with azospermia or by exclusion of men with a
sperm count below 20 mill/mL. This had an adverse effect on the
correlations, although they were still significant.
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Blood parameters of the participating men from the two centres are
shown in Table 2. The differences in
serum FSH and inhibin B levels between men from the two centres were
statistically significant, whereas there was no significant difference
in LH and testosterone levels (Table 2).
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Discussion |
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TopAbstractIntroductionSubject and MethodsResultsDiscussionReferences |
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The study gave us, however, an opportunity to compare reproductive hormones in two populations of normal men with different semen quality. Interestingly, men from centre A who had significantly higher sperm concentration also had significantly higher inhibin B and lower FSH levels than did men from centre B, after controlling for hour of sampling and diseases of the reproductive organs. The fact that serum inhibin B and FSH point in the same direction strengthen our findings and indicate that both serum markers may be useful proxy measures of spermatogenic potential in population studies. In fact, the predictive power in detecting oligospermia (semen concentration below 20 mill/mL), among men with a serum inhibin B below 80 pg/L and a serum FSH above 10 IU/L, was 100%.
We do not believe that the observed differences in serum levels of FSH and inhibin B can be explained by differences in the hour of sampling. Blood samples were generally drawn in the late morning at centre B and in the early afternoon at centre A. Several studies have found decreasing testosterone concentrations during the day (12, 13, 14), but no clear pattern regarding FSH secretion has been found (12, 15, 16, 17, 18). No report on the secretion pattern of inhibin B has been published.
Inhibin B is a marker of Sertoli cell function. Because the
Sertoli cells can only support, and thereby help, the maturing of a
given number of spermatozoas, serum inhibin B is probably a more direct
marker of spermatogenesis than is FSH, which has been used
traditionally as a marker of spermatogenesis in the clinical evaluation
of male infertility. Serum FSH levels are not only determined by the
testis but are also influenced by hypothalamic function. However,
measurement of inhibin has previously been problematical. Inhibin is a
glycoprotein dimer, consisting of two disulphides linked subunits (
and either ßA or ßB) (19). In addition to
the bioactive inhibin A (-ßA) and inhibin B
(-ßB) dimers, biologically inactive inhibin forms,
such as free inhibin subunits and unprocessed or partially processed
inhibin forms, are also present in the circulation (20, 21, 22). The first
inhibin assays developed could not distinguish between the bioactive
and inactive forms of inhibin. Studies that used these assays failed to
observe an inverse relationship between circulating inhibin and FSH
levels in different testicular disorders, presumably because the
results obtained with these assays did not reflect the level of
bioactive inhibin present in the circulation (23, 24).
The inhibin B assay used in this study was recently developed. It specifically measures the bioactive inhibin B dimer (8). Inhibin B is the main circulating inhibin form in adult men, and an inverse relationship exists between circulating inhibin B and FSH, both in men with normal and abnormal spermatogenesis (4, 5). We found a significant correlation between the serum FSH and inhibin B levels.
In conclusion, we have used serum levels of inhibin B and FSH as biomarkers of spermatogenesis to confirm a difference in semen quality between two groups of normal Danish men. Our findings suggest that serum inhibin B, in addition to FSH,, may serve as a new marker of spermatogenesis in future population studies on male reproductive health of normal men.
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Acknowledgments |
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Footnotes |
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Received June 13, 1997.
Revised August 18, 1997.
Accepted September 9, 1997.
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References |
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TopAbstractIntroductionSubject and MethodsResultsDiscussionReferences |
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