Impaired semen quality associated with environmental DDT exposure in young men living in a malaria area in the Limpopo Province, South Africa

Abstract

ABSTRACT:The pesticide DDT [1,1,1‐trichloro‐2,2‐bis(chlorodiphenyl)ethane] is 1 of the 12 persistent organic pollutants (POPs) under negotiation at the Stockholm Convention to restrict or ban their production and use because of their toxicity, resistance to breakdown, bioaccumulation, and potential for being transported over long distances. DDT has estrogenic potential, and the main metabolite,p,p′‐dichlorodiphenyl‐dichloroethylene (p,p′‐DDE), is a potent antiandrogen. In response to mounting evidence on the endocrine‐disrupting influence of environmental chemicals on human health, this epidemiological study was initiated to test the hypothesis that nonoccupational exposure to DDT affects male reproductive parameters. In a cross‐sectional study, healthy male subjects (n = 311) between 18 and 40 years (23 ± 5) of age were recruited from 3 communities in an endemic malaria area in which DDT is sprayed annually. A semen analysis according to World Health Organization (WHO) standards was performed. The Hamilton Thorne Computer Assisted Sperm Analysis (CASA) system was simultaneously used to determine additional sperm motility parameters. Blood plasma samples were assayed for p,p′‐DDT and metabolites as a measure of exposure. The exposure levels were expressed as lipid‐adjusted p,p′‐DDT and p,p′‐DDE values. The mean p,p′‐DDT and p,p′‐DDE concentrations were 90.23 μg/g(±102.4) and 215.47 μg/g(±210.6), respectively. The multivariate linear regression analyses indicated that mean CASA motility was lower with a higher p,p′‐DDE concentration (β = −0.02,P= .001) and the CASA parameter beat cross‐frequency (BCF) was higher with a higher p,p′‐DDT concentration (β = 0.01,P= .000). There was also a statistically significant positive association between percent sperm with cytoplasmic droplets and p,p′‐DDT concentration (β = 0.0014,P= .014). The ejaculate volume (mean 1.9 ± 1.33 mL) was lower than the normal range (≥2.0 mL) according to WHO, and a significant decrease with increasing p,p′‐DDE values was seen for both square root—transformed volume (β = −0.0003;P= .024) and count (β = −0.003;P= .04). Although there were no associations between either p,p′‐DDT or p,p′‐DDE concentrations and the rest of the seminal parameters, the incidence of teratozoospermia (99%; normal sperm <15%) was high. Twenty‐eight percent of the study group presented with oligozoospermia (<20 × 10 6 sperm/mL), which had a significant positive association with p,p′‐DDE (odds ratio [OR] = 1.001,P= .03). There was a significant positive association between participants with asthenozoospermia (32%) and p,p′‐DDT (OR 1.003,P= .006) and p,p′‐DDE (OR 1.001,P= .02). The results imply that nonoccupational exposure to DDT is associated with impaired seminal parameters in men. The high exposure levels of p,p′‐DDT and p,p′‐DDE are of concern because these levels could have far‐reaching implications for reproductive and general health.