The studies, published online today (Thursday 28 April) in Europe's leading reproductive medicine journal Human Reproduction, suggest that environmental pollutants could be changing the ratio of sperm carrying the X or Y (sex determining) chromosomes and that they could be contributing towards male reproductive disorders.
A study by Swedish researchers[1] is the first to show that exposure to persistent organochlorine pollutants (POPs) can affect the distribution of sex chromosomes in sperm, leading to a slight increase in the number of sperm bearing the Y chromosome
Aleksander Giwercman, professor of andrology at the Scanian Andrology Centre, Fertility Centre, Malmö University Hospital, Lund University, Sweden, and his colleagues looked at the effect of two POPs (CB-153 and DDE) on semen in 149 Swedish fishermen, aged between 27 and 67, some of whom fished off the east coast in the contaminated Baltic Sea, while others fished off the west coast.
Prof Giwercman explained: "Closed aquatic ecosystems, such as the Baltic Sea, have become heavily polluted by POPs. In spite of decreases since the 1970s, this contamination has resulted in higher levels of POPs in humans, such as fishermen, who consume large quantities of local fatty fish."
POPs enter the environment in a number of ways. Tarmo Tiido, co-author and PhD student at the Fertility Centre, said: "The sources of contamination for POPs are closely related to human activities such as domestic and industrial discharge, automobile exhausts, street run-off, slum sewage and agricultural chemicals. POPs from polluted soils are washed off the land into the sea. Additionally, the atmosphere plays an important role in their transport over long distances. POPs have a strong tendency to bioaccumulate in marine and terrestrial food webs. Humans, being at the top of the food web, particularly are exposed to POPs."
The researchers found that larger amounts of both CB-153 and DDE in the blood of the fishermen was associated with a statistically significant increase in the proportion of Y chromosome bearing sperm in semen, and that age, smoking and hormone levels had no effect.
"When we compared the 20% of fishermen with the highest exposure with the 20% with the lowest exposure, DDE was associated with an increase of 1.6% in sperm with Y chromosomes and CB-153 with an increase of 0.8%. To our knowledge this is the first study to show that the distribution of the sex chromosomes in sperm can be affected by exposure to POPs," said Prof Giwercman.
The study did not enable them to discover whether the increase in Y chromosome sperm would lead to an increase in boys being born, or what might be the mechanism involved. "We need a much larger population in order to investigate the implications of these changes on sex ratio of offspring as the number of children born to these fishermen was small.
"However, we think the fact that exposure to environmentally derived chemicals can change the sex chromosome ratio in sperm is worrying in itself and requires more attention from scientists and the public," said Prof Giwercman.
The second study by researchers from Denmark, Lithuania and Finland[2] suggests that a higher than expected prevalence of cryptorchidism (undescended testes) in Lithuania could be occurring because changing environmental factors are affecting the reproductive development of male foetuses.
Babies born with undescended testes are at higher risk of developing testicular cancer between the ages of about 20 and 40, and of having infertility problems. Cryptorchidism is one of the symptoms of testicular dysgenesis syndrome (TDS) – a collection of male reproductive disorders, possibly caused by errors in development of the foetal testes.
The Lithuanian study investigated 1,204 boys born in one hospital in Lithuania between October 1996 and November 1997. The boys were examined at birth and one year later. Sixty-nine (5.7%) of the boys had one or both testes undescended. After one year the testes had descended fully in 51 of the 68 children (75%) who were followed up, reducing the overall rate of the condition from 5.7% to 1.4%.
Dr Niels Jorgensen, one of the authors, said the study was significant because existing data on male reproductive health in Lithuania showed that the incidence of testicular cancer was one of the lowest in Europe and that semen quality in young men was good – a similar situation to that in Finland. "However, our results showed that the prevalence of cryptorchidism at birth in Lithuania was 5.7%, which was lower than in Denmark (9%), but higher than Finland (2.4%). These figures are not consistent with the data on semen quality and testicular cancer in the Nordic-Baltic region. Based on these data, we could have expected the frequency of cryptorchidism in Lithuanian boys to be similar to that in Finnish boys."
So what could be the reason for the discrepancy between these different indicators for male reproductive health?
Dr Jorgensen said: "Recent data show that semen quality and testicular cancer development is probably determined during the foetal period, but clinically this is usually not detected until the third decade of life. Thus, the recent findings of good semen quality and low frequency of testicular cancer in Lithuania may reflect the intrauterine environment situation more than 20 years ago. However, cryptorchidism can be detected immediately after birth and therefore the prevalence of congenital cryptorchidism detected in this study may be a better reflection of the current environmental situation than semen quality and the incidence of testicular cancer.
"If the hypothesis is correct that TDS is caused by environmental conditions, possibly interacting with genetic factors, the question arises as to whether adverse changes in the environmental factors affecting male reproductive health have taken place in Lithuania in the last 20 years.
"We need to look more closely at the role of environmental factors, including those that can disrupt the hormone system, and the role of genetics, lifestyle and other factors."
The study found that cryptorchidism was associated with low birth weight, preterm delivery, small gestational weight and other congenital abnormalities of the genitalia. An interesting significant risk factor was the father's weight; babies born to underweight fathers (body mass index less than 20kg/m2) were six times more likely to have undescended testes.
However, Dr Jorgensen said: "This finding should be treated with caution because the number of cases was rather low and only larger studies will be able to show whether this is a genuine association or not."
The study did not find a statistically significant difference between boys born to mothers who smoked or who worked in a potentially harmful environment where they might be exposed to heat, vibration or chemical, but the prevalence of cryptorchidism was slightly higher. It rose from 5.1% in non-smoking mothers to 7.8% in smoking mothers, and from 4.9% to 7.13% for mothers working in a potentially harmful environment.
"Although this increased risk was not statistically significant, it suggests that environmental factors could be important," said Dr Jorgensen.
[1] Exposure to persistent organochlorine pollutants associates with human sperm Y:X chromosome ratio. Human Reproduction. doi:10.1093/humrep/deh855
[2] Higher than expected prevalence of congenital cryptorchidism in Lithuania: a study of 1204 boys at birth and 1 year follow-up. Human Reproduction. doi:10.1093/humrep/deh887
Journal
Human Reproduction