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      Serum Dioxin-like Activity Is Associated with Reproductive Parameters in Young Men from the General Flemish Population

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          Abstract

          Background

          2,3,7,8-Tetrachlorodibenzo- p-dioxin (TCDD) and some related environmental contaminants are aryl hydrocarbon receptor (AhR) ligands that exert reproductive and developmental toxicity in laboratory animals. In humans, fertility-related effects are less documented.

          Objective

          The aim of this study was to investigate the relationship between dioxin-like biological activity in serum and parameters of reproductive status in men from the general population 5 months after a polychlorinated biphenyl and dioxin food-contamination episode in Belgium.

          Design

          In the framework of the cross-sectional Flemish Environment and Health Study (FLEHS), we recruited 101 men 20–40 years of age and evaluated sperm parameters, measured sex hormones, and gathered information on a number of lifestyle factors. In addition, we determined the AhR-mediated enzymatic response elicited by individual serum samples and expressed it as TCDD equivalent concentrations (CALUX-TEQs) using an established transactivation assay.

          Results

          Age ( p = 0.04) and the frequency of fish ( p = 0.02) and egg ( p = 0.001) consumption were independent positive determinants of serum dioxin-like activity. After correcting for possible confounders, we found that a 2-fold increase in CALUX-TEQ > 16 pg/L was associated with a 7.1% and 6.8% (both p = 0.04) decrease in total and free testosterone, respectively. We also observed a more pronounced drop in semen volume of 16.0% ( p = 0.03), whereas sperm concentration rose by 25.2% ( p = 0.07). No relationship was found with total sperm count or sperm morphology.

          Conclusions

          These data suggest an interaction of dioxin-like compounds with the secretory function of the seminal vesicles or prostate, possibly indirectly through an effect on testosterone secretion, at levels not affecting spermatogenesis as such.

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          Most cited references48

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          Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), and related compounds: environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs).

          S H Safe (1989)
          Halogenated aromatic compounds, typified by the polychlorinated dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), biphenyls (PCBs), and diphenylethers (PCDEs), are industrial compounds or byproducts which have been widely identified in the environment and in chemical-waste dumpsites. Halogenated aromatics are invariably present in diverse analytes as highly complex mixtures of isomers and congeners and this complicates the hazard and risk assessment of these compounds. Several studies have confirmed the common receptor-mediated mechanism of action of toxic halogenated aromatics and this has resulted in the development of structure-activity relationships for this class of chemicals. The most toxic halogenated aromatic is 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and based on in vivo and in vitro studies the relative toxicities of individual halogenated aromatics have been determined relative to TCDD (i.e., toxic equivalents). The derived toxic equivalents can be used for hazard and risk assessment of halogenated aromatic mixtures; moreover, for more complex mixtures containing congeners for which no standards are available (e.g., bromo/chloro mixtures), several in vitro or in vivo assays can be utilized for hazard or risk assessment.
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            Paternal concentrations of dioxin and sex ratio of offspring.

            2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD or dioxin), is commonly considered the most toxic man-made substance. We have previously shown that high serum concentrations of TCDD in parents from Seveso, Italy, were linked to their having a relative increase in the number of female births after the parents exposure to a release of dioxin in 1976. We have continued the study to determine whether the parents' sex and/or age at exposure affected the sex ratio of their children. We measured the TCDD concentrations in serum samples from potentially exposed parents collected in 1976 and 1977, and investigated the sex ratio of their offspring. Serum samples were collected from 239 men and 296 women. 346 girls and 328 boys were born to potentially exposed parents between 1977 and 1996, showing an increased probability of female births (lower sex ratio) with increasing TCDD concentrations in the serum samples from the fathers (p=0.008). This effect starts at concentrations less than 20 ng per kg bodyweight. Fathers exposed when they were younger than 19 years of age sired significantly more girls than boys (sex ratio 0.38 [95% CI 0.30-0.47]). Exposure of men to TCDD is linked to a lowered male/female sex ratio in their offspring, which may persist for years after exposure. The median concentration of dioxin in fathers in this study is similar to doses that induce epididymal impairments in rats and is about 20 times the estimated average concentration of TCDD currently found in human beings in industrialised countries. These observations could have important public-health implications.
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              Effects of male age on semen quality and fertility: a review of the literature.

              To review the literature on the association between male age and semen quality (semen volume, concentration, motility, and morphology) and fertility status (pregnancy rate and time to pregnancy/subfecundity). Review of English language-published research over the last 20 years from January 1, 1980, through December 31, 1999, using MEDLINE and Biosis databases. Studies with insufficient numbers of subjects, case reports, case series, or anecdotal data were excluded. Among the methodologically stronger studies, decreases in semen volume of 3%-22%, decreases in sperm motility of 3%-37%, and decreases in percent normal sperm of 4%-18% were likely when comparing 30-year-old men to 50-year-old men. Most studies examining fertility status suggest a relationship between male age and fertility, but the results are most likely confounded by female partner age. Among studies that did control for female age, comparisons between men under 30 and men over 50 found relative decreases in pregnancy rates between 23% and 38%. A comparison of the various age categories showed that the increased risks for subfecundity ranged from 11% to 250%. The weight of the evidence suggests that increased male age is associated with a decline in semen volume, sperm motility, and sperm morphology but not with sperm concentration.
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                Author and article information

                Journal
                Environ Health Perspect
                Environmental Health Perspectives
                National Institute of Environmental Health Sciences
                0091-6765
                November 2006
                27 July 2006
                : 114
                : 11
                : 1670-1676
                Affiliations
                [1 ] Department of Endocrinology, University Hospital Ghent, Belgium
                [2 ] Study Centre for Carcinogenesis and Primary Prevention of Cancer, Department of Radiotherapy, Nuclear Medicine and Experimental Cancerology, University Hospital Ghent, Belgium
                [3 ] Flemish Institute of Technological Research (VITO), Centre of Expertise in Environmental Toxicology, Mol, Belgium
                [4 ] Provincial Institute for Hygiene, Antwerp, Belgium
                [5 ] Department of Human Heredity, Catholic University of Leuven, Leuven, Belgium
                Author notes
                Address correspondence to W. Dhooge, Department of Endocrinology, University Hospital Ghent, 185 De Pintelaan, B9000 Ghent, Belgium. Telephone: 32 9 241 80 46. Fax: 32 9 241 80 40. E-mail: Willem@ 123456Dhooge.org
                [*]

                F. Buntinx, S. Callens, E. Den Hond, R. Fagard, T. Nawrot, L. Thijs, J.A. Staessen, D. Vanderschueren, E. Van Hecke, H. Van Loon, and M.K. Viaene (Catholic University of Leuven, Leuven, Belgium); T. De Ceuster, E. Goelen, R. Van Den Heuvel, G. Verheyen, and L. Verschaeve [Flemish Institute of Technological Research (VITO), Mol, Belgium]; I. Loots, M. Herremans, P. Mertens, P. Vermeire, and J. Weyler (University of Antwerp, Antwerp, Belgium); and H.A. Roels (Université catholique de Louvain, Brussels, Belgium).

                The authors declare they have no competing financial interests.

                Article
                ehp0114-001670
                10.1289/ehp.9224
                1665408
                17107851
                7a93f7a6-fcd1-45d0-b903-473904669b68
                This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original DOI
                History
                : 1 April 2006
                : 27 July 2006
                Categories
                Research

                Public health
                dioxin,sperm concentration,tcdd,hormones,egg consumption,dr-calux,testosterone,semen volume,male fertility

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