New research has shown that women who ate a lot of beef while pregnant had sons who were more likely to suffer from poor sperm quality as adults, and it suggests that the growth promoters used in cattle may play a role in these men’s reduced fertility.
The study [1] of men living in the USA and born between 1949 and 1983 revealed that those whose mothers ate more than seven beef meals a week had a sperm concentration that was over 24% lower than in men whose mothers ate less beef. In addition, three times more sons of high beef consumers had a sperm concentration that would be classified as sub-fertile according to World Health Organization standards, in comparison to men whose mothers ate less beef.
Professor Shanna Swan, the lead author of the study that is published online in Human Reproduction journal today (Wednesday 28 March), said: "These findings suggest that maternal beef consumption is associated with lower sperm concentration and possible sub-fertility, associations that may be related to the presence of anabolic steroids and other xenobiotics in beef."
In the Associate Editor’s Commentary to the study [2], Frederick vom Saal, professor of biology at the University of Missouri, Columbia, USA, warned that if foreign chemicals (xenobiotics) such as anabolic steroids were involved in reducing sperm quality, it could be just "the tip of the iceberg" and that the xenobiotics might be involved in other reproductive problems as well.
"Furthermore, women would also be expected to be affected by developmental exposure to xenobiotic hormones; studies relating maternal beef consumption to daughters’ incidence of polycystic ovarian syndrome, age at puberty and postnatal growth rate would be predicted to show a significant relationship," he said.
Growth promoters for cattle, such as the synthetic hormone diethylstilbestrol (DES), have been used in the USA since 1954. Although DES was banned for use in cattle in 1979, other hormones such as oestradiol, testosterone, progesterone, zeranol, trenbolone acetate and melengestrol continue to be used. Residues of these chemicals remain in the meat after slaughter and so, in the USA, the FDA has regulated their use to avoid unintended adverse effects in humans eating the meat and defined an "acceptable daily intake". The International Joint Food and Agricultural Organization’s World Health Organization Expert Committee on Food Additives (JECFA) has also published ADIs. In Europe, the use of these hormones has been banned since 1988.
"These ADIs are based on traditional toxicological testing, and the possible effects on human populations exposed to residues of anabolic sex hormones through meat consumption have never, to our knowledge, been studied. Theoretically, the foetus and young children are particularly sensitive to exposure to sex steroids. Therefore, the consumption of residues of steroids in meat by pregnant women and young children is of particular concern," said Prof Swan, who is director of the Center for Reproductive Epidemiology, associate chair for research and professor of obstetrics and gynecology at the University of Rochester School of Medicine and Dentistry.
Prof Swan and her colleagues recruited couples to the study when the pregnant women attended prenatal clinics between 1999 and 2005. As well as asking questions about the couples themselves (medical histories, lifestyle factors such as smoking, alcohol consumption and diet), the researchers requested the men to ask their mothers to fill in a brief questionnaire about their diet while pregnant with their sons. The men also provided semen samples.
Out of 773 men who provided semen samples, information was available for 387 on how many beef meals their mothers ate during their pregnancies. On average, the mothers ate 4.3 beef meals a week; only 15 (4%) reported eating no beef during pregnancy; 336 ate seven or fewer beef meals a week; 51 reported eating more than seven beef meals a week. Women who were "high beef consumers" also ate more other red meat and were more likely to be living in North America at the time their son was born [3].
Prof Swan said: "The number of beef meals consumed by the mother was significantly and inversely related to her son’s sperm concentration. Sons of high beef consumers had an average sperm concentration of 43.1 million sperm per millimetre of seminal fluid, while sons of mothers who ate less beef had an average of 56.9 million sperm – a statistically significant difference of 24.3%. Among sons of mothers whose beef consumption was not high, only 5.7% had sperm concentration below the WHO threshold for sub-fertility of 20 million sperm per millimetre of seminal fluid. This was significantly less than the 17.7% of men whose mothers were high beef consumers who fell below this threshold.
"The proportion of men with sub-fertile sperm concentration and of men with a history of possible sub-fertility increased the more beef meals the mothers had eaten while pregnant. These findings suggest that maternal beef consumption is associated with lower sperm concentration and possible sub-fertility – associations that may be related to the presence of anabolic steroids and other xenobiotics in beef.
"However, I must point out that most mothers in this study lived in North America and our findings may not apply to other regions of the world where beef is produced by other methods. In addition, pesticides, other contaminants and lifestyle factors correlating with greater beef consumption may play a role in the effect we observed.
"In order to clarify whether prenatal exposure to anabolic steroids is responsible for our findings, this study needs to be repeated in men born in Europe after 1988 when growth promoters were no longer permitted in beef sold or produced there."
The men’s own beef consumption correlated weakly with their mothers’ and was unrelated to their sperm concentration, suggesting that the men’s own diet of beef did not have an impact on their sperm quality.
In his commentary, Prof vom Saal said there was increasing evidence that xenobiotics can cause more damaging effects in humans if exposure occurs while a child is still developing in its mother’s womb, than can be revealed by the traditional toxicology tests. "There is an entirely different view today, concerning the potential for harm from developmental exposure to very low doses of xenobiotics relative to the data available to JECFA based on research focusing on mutagenesis conducted in the 1970 and early 1980s," he said. He called on the JECFA and other regulatory bodies to revisit the risks associated with exposure during foetal development to hormonal residues in beef.
He concluded: "Given the importance of this issue, the intriguing relationship reported by Swan and colleagues should serve to stimulate further research to investigate the basis for the association between maternal beef consumption during pregnancy and sperm concentration in male offspring."
[1] Semen quality of fertile US males in relation to their mothers’ beef consumption during pregnancy. Human Reproduction. doi:10.1093/humrep/dem068
[2] Associate editor’s commentary on the article ‘Semen quality of fertile US males in relation to their mothers’ beef consumption during pregnancy’. Could hormone residues be involved? Human Reproduction. doi:10.1093/humrep/dem092
[3] Other red meat was much less likely to have been treated with growth promoters at this time. Moreover, beef predominated among the meats the mothers consumed. The researchers found a much weaker, non-significant association between number of meals of other red meat and sperm concentration.
Journal
Human Reproduction