Semen Quality of Fertile U.S. Males in Relation to Their Mothers' Beef Consumption during Pregnancy

S.H. Swan; F. Liu; J.W. Overstreet; C. Brazil; N.E. Skakkebaek


Hum Reprod. 2007;22(6):1497-1502. 

In This Article

Abstract and Introduction

Background: To look at possible long-term risks from anabolic steroids and other xenobiotics in beef, we examined mens' semen quality in relation to their mother's self-reported beef consumption during pregnancy.
Methods: The study was carried out in five US cities between 1999 and 2005. We used regression analyses to examine semen parameters in 387 partners of pregnant women in relation to the amount of beef their mothers reported eating while pregnant. Mothers' beef consumption was also analysed in relation to the son's history of previous subfertility.
Results: Sperm concentration was inversely related to mothers' beef meals per week (P = 0.041). In sons of 'high beef consumers' (> 7 beef meals/week), sperm concentration was 24.3% lower (P = 0.014) and the proportion of men with sperm concentration below 20 × 106/ml was three times higher (17.7 versus 5.7%, P = 0.002) than in men whose mothers ate less beef. A history of previous subfertility was also more frequent among sons of 'high beef consumers' (P = 0.015). Sperm concentration was not significantly related to mother's consumption of other meat or to the man's consumption of any meat.
Conclusions: These data suggest that maternal beef consumption, and possibly xenobiotics in beef, may alter a man's testicular development in utero and adversely affect his reproductive capacity.

Diethylstilbestrol (DES), the first synthetic hormone, was formulated in 1933 and was rapidly marketed for a wide range of medical indications (Swan, 2000). In 1947, the year that DES was approved for use by pregnant women, investigators at Purdue University demonstrated the ability of this synthetic hormone to stimulate growth in cattle (Raun and Preston, 2002). In 1954, the US Food and Drug Administration (FDA) approved DES for use in cattle, and by 1956 more than two-thirds of the nation's feeder cattle were receiving DES (Marcus, 1994). Simultaneously, other hormonal additives were being tested for use in cattle; between 1956 and 1958, estradiol benzoate and progesterone implants were approved, first for use in steers and then heifers. Approval for use of other anabolic hormones in cattle followed rapidly. While the US FDA withdrew approval of DES for use in cattle in 1979, other anabolic hormones continue to be used legally in the USA and elsewhere as growth promoters in meat production. Six hormones are now in common use in Canada and USA: the three natural steroids, estradiol, testosterone and progesterone, and the three synthetic hormones, zeranol (an estrogen), trenbolone acetate (a steroid with androgen and glucocorticoid action) and melengestrol acetate (a potent progestin) (Meyer, 2001). The anabolic steroids are most often used in combination; often an androgen and estrogen are used simultaneously, e.g. estradiol and trenbolone acetate. 'Good veterinary practice' prescribes that melengestrol acetate be given in the feed and the other hormones given as capsules implanted subcutaneously in the calf's ear from where the hormones continuously are released into circulation. All six hormones can induce increased growth and development of the animal by mechanisms similar to that of the 'peripheral' form of human precocious puberty, which is also associated with a growth spurt (Parent et al., 2003). At slaughter, not all steroids have been metabolized or excreted; measurable levels are, in fact, present in muscle, fat, liver, kidney and other organs present in meat products (Henricks et al., 2001). Therefore, it has been necessary to regulate the use of these growth promoters to avoid unintended adverse effects in humans eating these meat products. FDA has defined an 'acceptable daily intake' (ADI) for each of these veterinary drugs (Henricks et al., 2001), and since 1988 the use of these hormones has been banned in Europe (Stephany, 2001). The International Joint Food and Agricultural Organization's World Health Organization Expert Committee on Food Additives (JECFA) has also published ADIs for all hormones in current use on the basis of animal testing.

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 fetus and the prepubertal child are particularly sensitive to exposure to sex steroids (Andersson and Skakkebæk, 1999; Bay et al., 2004). Therefore, the consumption of residues of steroids in meat by pregnant women and young children is of particular concern. Recent animal and human studies have suggested that perinatal exposures, including exposure to sex steroids, can induce a testicular dysgenesis syndrome (Skakkebæk et al., 2001), and result in a number of testicular disorders in adulthood, including poor spermatogenesis.

The lack of human data on the safety of anabolic steroids in meat production prompted us to analyse mother's beef consumption while pregnant in relation to her son's semen parameters in a large multicenter pregnancy cohort study, the Study for Future Families (SFF).


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