Poor semen quality may contribute to recent decline in fertility rates
Tina Kold Jensen1,2,7,
Elisabeth Carlsen1,
Niels Jørgensen1,
Jørgen G. Berthelsen3,
Niels Keiding4,
Kaare Christensen5,
Jørgen Holm Petersen1,4,
Lisbeth B. Knudsen6 and
Niels E. Skakkebæk1
1 Department of Growth and Reproduction, Rigshospitalet, The Juliane Marie Centre, section GR-5064, Blegdamsvej 9, DK-2100 Copenhagen,
2 University of Southern Denmark, Department of Environmental Medicine, Winsloewsparken 17, 5000 Odense C,
3 Department of Obstetrics and Gynaecology, Hillerod Hospital, DK-3400 Hillerod,
4 Department of Biostatistics, University of Copenhagen, Blegdamsvej 3, DK-2200 Copenhagen,
5 University of Southern Denmark, Department of Epidemiology, Sdr. Boulevard, 5000 Odense C,
6 Danish Centre for Demographic Research, University of Southern Denmark, Sdr. Boulevard, 5000 Odense C, Denmark.
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Abstract
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During past decades, we have witnessed a remarkable decline in fertility rates (number of births per 1000 women of reproductive age) in the industrialized world. It seems beyond doubt that the enormous social changes of our societies play the major role in this decline, but can it be attributed to changing social structures alone or is a reduced fecundity in the population also a factor? To address this we have focused on trends in teenage pregnancies (which to a large extent are unplanned). During the period in question fertility rates among 1519 year old Danish women have been falling and the decline in fertility rate is not counterbalanced by an increase in the rate of induced abortion. When seen together with recent results from Denmark, which have shown that more than 30% of 19 year old men from the general population now have sperm counts in the subfertile range, we argue that this fall may not be attributable to social factors, changes in conceptive practices or diminished sexual activity alone. It seems reasonable also to consider widespread poor semen quality among men as a potential contributing factor to low fertility rates among teenagers. Due to the concern caused by the low sperm count among younger Danish men, the Danish Ministries of Health and Environment have launched a surveillance programme which includes an annual examination of the semen quality in 600 young Danes from the general population. We propose that researchers in other countries with low and falling fertility rates among young women should consider the possibility that semen quality of their younger male cohorts may also have deteriorated.
Key words:
Denmark/fecundity/fertility rates/semen quality
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Introduction
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During past decades we have witnessed a remarkable decline in fertility rates (number of births per 1000 women in reproductive age) in the industrialized world (United Nations, 1997; Kaufmann et al., 1998
; Pearce et al., 1999
). In most areas, including several European countries and Japan, women have an average of less than two children (Central Intelligence Agency, 2001
) which is too low to sustain the population at the current level; in Spain and Italy this figure is as low as 1.2 (Bosch, 2000
). Most demographers and social scientists believe that the decline is caused by the changing social structures of the western world. It seems beyond doubt that the enormous social changes of our societies play the major role. Women (couples) benefit from more effective contraception to delay childbearing due to education and they often take active part in the labour force before considering having a family. In Denmark the average age of a woman at birth of first child is 28 years at present and fertility rates are declining among women aged 1524 years but increasing among older women (Figures 1 and 2
) (Knudsen, 1999
).

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Figure 1. Fertility rates (number of births per 1000 women aged 2024 years), abortion rates (number of abortions per 1000 women aged 2024 years) and pregnancy rate (fertility and abortion rate) among 2024 year old women in Denmark from 19851999.
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Figure 2. Fertility rates (number of births per 1000 women aged 2549 years), abortion rates (number of abortions per 1000 women aged 2549 years) and pregnancy rate (fertility and abortion rate) among 2549 year old women in Denmark from 19851999.
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The question is whether the decreasing number of births can be attributed to changing social structures alone. It appears that we should also consider the possibility that decreased fecundity (ability to conceive) may contribute to the decreasing fertility rate. A Danish questionnaire study of young women showed that the desired average family size was two children (Bertelsen and Ussing, 1974
), but nevertheless when the women born in the same years as those who answered the questionnaire were followed in registers, the cohorts had given birth to fewer children than this desired number (Knudsen, 1993
). And indeed, infertility treatment has become an increasing part of the health care system. In Denmark in 1997, 2.6% of all children were born after the use of assisted reproductive technology (Nygren and Andersen, 2001
). In addition, an established 1.3% of all children are born after artificial insemination with donor or husband semen. Furthermore, most recent data from the Danish Fertility Society (A.Nyboe Andersen, personal communication) have shown that the number of pregnancies after assisted reproductive technology has increased by 19% from 1997 to 1999 and the number of children born after assisted reproductive technology may therefore approach 5% of all births. This increase could be due to an increase in the number of infertile couples but could also be caused by more couples seeking treatment and even better success rates. Indeed, some population studies have reported no decline or even an increase in fecundity with calendar time (Mosher, 1985
; Templeton et al., 1990
; Akre et al., 1999
; Joffe, 2000
). However one study among 400 000 pregnant Swedish women (Akre et al., 1999
) did not take into account truncation bias at both ends of the study period, which occurs when a calendar-time cut-off date is imposed (e.g. when data were collected), after which pregnancies are no longer included. This bias has the effect of artificially over-estimating fecundity in the most recent category (Jensen et al., 2000
).
A crucial question, however, seems to be whether there is any relationship between the recent controversial reports on declining semen quality (Carlsen et al., 1992
; Auger et al., 1995
; Olsen et al., 1995
; Bujan et al., 1996
; Fisch et al., 1996
; Irvine et al., 1996
; Paulsen et al., 1996
; Swan et al., 1997
) and the observed decrease in fertility rates. Theoretically, fecundity may be unaffected by a reduction in sperm concentration until a certain lower threshold is reached. However, it appears from a Danish study of 1820 year old men from the general population that we may have reached that threshold level. In the study which included 708 Danish men from two cities (Copenhagen and Aalborg), 21% had sperm counts <20x106/ml (lower WHO limit) (World Health Organization, 1992
) and 43% <40x106/ml (Andersen et al. 2000
). The latter number is noteworthy because another study indicated that men with sperm counts <40x106/ml had reduced fecundity (prolonged waiting time to pregnancy) (Bonde et al., 1998a
).
In addition, evidence is emerging that semen quality is lower among younger cohorts. A meta-analysis of semen quality of normal Danish men suggested a birth-cohort related decline in semen quality (Bonde et al., 1998b
) and the trend seems to continue as the younger cohorts born around 1980, had the lowest sperm counts of all cohorts examined (Figure 3
) (Andersen et al., 2000
).

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Figure 3 . Median sperm concentration and 2575 percentiles according to year of birth from 10 Danish studies of men born 19351975 (reconstructed from Bonde et al., 1998b) and 708 men from the general Danish population born 19791981 (Andersen et al., 2000 ).
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If the average younger man has a lower fecundity than the average older man, we might begin to see this reflected in the fertility rates. Perhaps this is what we are now witnessing. Generally, female partners are of the same age or younger and therefore a poor semen quality of the present male young cohorts should primarily be reflected in the fertility rates of the young female cohorts. In this respect the fertility rates of teenagers is particularly interesting as they reflect to a large extent unplanned pregnancies caused by lack of contraceptive use or contraceptive failure. A small and increasing percentage of Danish teenagers of whom most are from ethnic minority groups are however married and their fertility is very high. Nevertheless, in Denmark fertility rates among teenagers are showing a subtle, but constant fall (Figure 4
). Similar findings have been observed in many countries (Singh and Darroch, 2000
). The decline in birth rates among female teenagers is not counterbalanced by an increase in the rate of induced abortion in Denmark (which has been legal since 1973). Both abortion rates and the pregnancy rate (number of abortions and births per 1000 in the relevant population) have been decreasing among teenagers (Figure 4
). It is worth noticing that the national Danish data are valid and complete (Knudsen, 1993
). We argue that this fall may not be attributed to social factors alone or changes in contraceptive practices. The `morning after' pill has been advertised more during the last couple of years, although there are no official figures for its use among teenagers. Nevertheless, a recent study showed that the use of contraception and education levels among Danish teenagers during the past 10 years has remained largely unchanged (Frederiksberg Kommunes Sundhedsafdeling, 1999
). Neither is it likely that diminished sexual activity is the cause (Frederiksberg Kommunes Sundhedsafdeling, 1999
). It therefore seems particularly important to follow the younger cohorts to see whether their future fertility rates will be affected. Perhaps we may already be seeing some impact on the fertility, as the pregnancy rate among 2024 year olds, in contrast to those >25 years, has also been falling in last decade (Figure 1
).

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Figure 4. Fertility rates (number of births per 1000 women aged 1519 years), abortion rates (number of abortions per 1000 women aged 1519 years) and pregnancy rate (fertility and abortion rate) among 1519 year old women in Denmark from 19851999.
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Conclusion
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Recent trends towards lower fertility rates in Denmark, particularly among the youngest women are not fully explained. It seems reasonable, besides social factors, also to consider the recently reported low semen quality among young men as a potential contributing factor.
Due to the concern caused by the low sperm counts among younger Danish men, the Danish Ministries of Health and Environment have launched a surveillance programme which includes an annual examination of the semen quality in 600 young Danes from the general population. We propose that researchers in other countries with low and falling fertility rates among young women should consider the possibility that semen quality of their younger male cohorts may also have deteriorated.
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Notes
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7 To whom correspondence should be addressed. E-mail: tkjensen{at}health.sdu.dk 
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References
|
---|
Akre, O., Cnattingius, S., Bergström, R., Kvist, U., Trichopoulos, D. and Ekbom, A. (1999). Human fertility does not decline: evidence from Sweden. Fertil. Steril., 71, 10661069.[ISI][Medline]
Andersen, A.G., Jensen, T.K., Carlsen, E., Jorgensen, N., Andersson, A.M., Krarup, T., Keiding, N. and Skakkebaek, N.E. (2000) High frequency of sub-optimal semen quality in an unselected population of young men. Hum. Reprod., 15, 366372.[Abstract/Free Full Text]
Auger, J., Kunstmann, J.M., Czyglik, F. and Jouannet, P. (1995) Decline in semen quality among fertile men in Paris during the past 20 years. N. Engl. J. Med., 332, 281285.[Abstract/Free Full Text]
Bertelsen, O. and Ussing, J. (1974) Family size and lifestyle. Danish National Institute of Social Research, Copenhagen.
Bonde, J.P., Ernst, E., Jensen, T.K., Hjollund, N.H.I., Kolstad, H., Henriksen, T.B., Scheike, T., Giwercman, A., Olsen, J. and Skakkebæk, N.E. (1998a) The relation between semen quality and fertility. A population based study of 430 first-pregnancy planners. Lancet, 352, 11721177.[ISI][Medline]
Bonde, J.P., Jensen, T.K., Larsen, S.B., Abell, A., Scheike, T., Hjollund, N.H.I., Kolstad, H., Ernst,E., Giwercman, A., Skakkebæk, N.E. et al. (1998b) Year of birth and sperm count in 10 Danish occupational studies. Scand. J. Work Environ. Health, 24, 407413.[ISI][Medline]
Bosch, X. (2000) Spain faces massive decline in population. Br. Med. J. 320, 891.[Free Full Text]
Bujan, L., Mansat, A., Pontonnier, F. and Mieusset, R. (1996) Time series analysis of sperm concentration in fertile men in Toulouse, France between 1977 and 1992. Brit. Med. J., 312, 471472.[Abstract/Free Full Text]
Carlsen, E., Giwercman, A., Keiding, N. and Skakkebaek, NE. (1992) Evidence for decreasing quality of semen during past 50 years. Br. Med. J., 305, 609613.[ISI][Medline]
Central Intelligence Agency (2001) The World Fact Book, Bartleby.com.Inc., Washington D.C.
Fisch, H., Goluboff, E.T., Olson, J.H., Feldshuh, J., Broder, S.J., Barad, D.H. (1996) Semen analyses in, 1,283 men from the United States over a 25-year period: no decline in quality. Fertil. Steril., 65, 10091014.[ISI][Medline]
Frederiksberg Kommunes Sundhedsafdeling (1999) Young, 1999, a sexual profile (In Danish). Forebyggelsessekretariatet, Frederiksberg, Copenhagen, 1188.
Irvine, S., Cawood, E., Richardson, D., MacDonald, E. and Aitken, J. (1996) Evidence of deteriorating semen quality in the United Kingdom: birth cohort study in 577 men in Scotland over 11 years. Br. Med. J., 312, 467471.[Abstract/Free Full Text]
Jensen, T.K., Keiding, N., Scheike, T., Slama, R., Spira, A. et al. (2000). Declining human fertility (letter). Fertil. Steril., 73, 421423.
Joffe, M. (2000). Time trends in biological fertility in Britain. Lancet, 355, 19611965.[ISI][Medline]
Kaufmann, R.B., Spitz, A.M., Strauss, L.T., Morris, L., Santelli, J.S., Koonin, L.M. and Marks, J.S (1998) The decline in US teen pregnancy rates, 19901995. Pediatrics, 102, 11411147.[Abstract/Free Full Text]
Knudsen, L.B. (1993) Fertility Trends in Denmark in the 1980s. Statistiske Undersøgelser nr. 44. Danmarks Statistik, Copenhagen.
Knudsen, L.B. (1999) Recent fertility trends in Denmark A discussion of the impact of family policy in a period with increasing fertility. In Research Report 11. Danish Center for Demographic Research, University of Southern Denmark, Odense.
Mosher, W.D. (1985). Reproductive impairments in the United States, 19651982. Demography, 22, 415430.[ISI][Medline]
Nygren, K.G. and Andersen, A.N. (2001) Assisted reproductive technology in Europe, 1997. Results generated from European registers by ESHRE. European IVF-Monitoring Programme (EIM), for the European Society of Human Reproduction and Embryology (ESHRE). Hum. Reprod., 16, 384391.[Abstract/Free Full Text]
Olsen, G.W., Bodner, K.M. and Ramlow, J.M. (1995) Have sperm counts been reduced 50 percent in 50 years? a statistical model revisited. Fertil. Steril., 63, 887893.[ISI][Medline]
Paulsen, C.A., Berman, N.G. and Wang, C. (1996) Data from men in greater Seattle area reveals no downward trend in semen quality: further evidence that deterioration of semen quality is not geographically uniform. Fertil. Steril., 65, 10151020.[ISI][Medline]
Pearce, D., Cantisani, G. and Laihonon, A. (1999) Changes in fertility and family sizes in Europe. Popul. Trend, Spring, 3340.
Singh, S. and Darroch, J.E. (2000) Adolescent pregnancy and childbearing: levels and trends in developed countries. Fam. Plann. Perspect., 32, 1423.[ISI][Medline]
Swan, S.H., Elkin, E.P. and Fenster, L. (1997) Have sperm densities declined? A reanalyses of global trend data. Environ. Health Perspect., 105, 12281232.[ISI][Medline]
Templeton, A., Fraser, C. and Thompson, B. (1990). The epidemiology of infertility in Aberdeen. Brit. Med. J., 301, 148152.[ISI][Medline]
World Health Organization (1992) Who Laboratory Manual for the Examination of Human Semen and SpermCervical Mucus Interaction. Cambridge University Press, Cambridge.