Abstract
Due to the grasshopper effect, the Arctic food chain in Canada is contaminated with persistent organic pollutants (POPs) of industrial origin, including polychlorinated biphenyls and organochlorine pesticides. Exposure to POPs may be a contributor to the greater incidence of poor fetal growth, placental abnormalities, stillbirths, congenital defects and shortened lifespan in the Inuit population compared to non-Aboriginal Canadians. Although maternal exposure to POPs is well established to harm pregnancy outcomes, paternal transmission of the effects of POPs is a possibility that has not been well investigated. We used a rat model to test the hypothesis that exposure to POPs during gestation and suckling leads to developmental defects that are transmitted to subsequent generations via the male lineage. Indeed, developmental exposure to an environmentally relevant Arctic POPs mixture impaired sperm quality and pregnancy outcomes across two subsequent, unexposed generations and altered sperm DNA methylation, some of which are also observed for two additional generations. Genes corresponding to the altered sperm methylome correspond to health problems encountered in the Inuit population. These findings demonstrate that the paternal methylome is sensitive to the environment and that some perturbations persist for at least two subsequent generations. In conclusion, although many factors influence health, paternal exposure to contaminants plays a heretofore-underappreciated role with sperm DNA methylation contributing to the molecular underpinnings involved.
Highlights
The World Health Organization states that direct exposure to persistent organic pollutants (POPs), even at low doses, can lead to an increased risk of cancer, reproductive disorders, altered immune response, neuro-behavioural impairment and endocrine disruption [1,2]
Based on the observed developmental disorders and placental defects, reduced fetal growth, neonatal and postnatal mortality, congenital defects and delayed puberty, the compounds appear to produce effects that are in some cases strikingly similar to those experienced in Inuit [9,11,12]
This experimental approach may represent a good prognostic tool for anticipating human health problems that could arise from exposure to these organic pollutants, in the Inuit population
Summary
The World Health Organization states that direct exposure to persistent organic pollutants (POPs), even at low doses, can lead to an increased risk of cancer, reproductive disorders, altered immune response, neuro-behavioural impairment and endocrine disruption [1,2]. There are major health disparities between Inuit and non-Aboriginal Canadians such that the life expectancy is 14 years shorter among Inuit [9,10]. Stillbirths are 1.9 times more frequent among Inuit than non-Aboriginal residents in the Canadian province of Quebec and are attributed to poor fetal growth, placental and congenital disorders [12]. A study of northern Quebec Inuit communities revealed that prenatal exposure to POPs is correlated with shorter pregnancy and with lower infant birth weight, length and head circumference [12]. Lower alertness in Inuit infants [13], more frequent respiratory infections [14], and slower emotional development [15] in Inuit preschoolers have been correlated with in utero exposure to PCBs
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