Long-term food-exposure of zebrafish to PCB mixtures mimicking some environmental situations induces ovary pathology and impairs reproduction ability

Abstract

Although the use of polychlorinated biphenyls (PCBs) has been banned for several decades, they are still present in the environment and are occasionally mechanically released from sediment or transferred through the trophic chain. Field analyses have established correlations between exposure to PCBs and alterations in fish physiology including reproductive function. Experimental exposures have been mainly performed using dioxin-like PCBs or other congeners at very high concentrations. However, these studies are often difficult to relate to real-life conditions. In the present study, we performed a life-cycle exposure using zebrafish model and mixtures representative of some environmental situations in terms of doses, composition and containing mainly non dioxin-like congeners. Exposure was performed through diet which is the main contamination route in the field. We demonstrated a bioaccumulation of PCBs in males and females as well as a maternal transfer to the eggs. Survival, growth and organ size were similar for all conditions. Several reproductive traits were altered after exposure to a PCB-contaminated diet, including a reduction in the number of fertilized eggs per spawn as well as an increase of the number of poorly fertilized spawns. This latter observation was found irrespective of the sex of contaminated fish. This is related to modifications of ovary histology revealing a decrease of maturing follicles and an increase of atretic follicles in the ovaries of females exposed to PCBs. These results indicate that exposure to PCBs mixtures mimicking some environmental situations, including mainly non dioxin-like congeners, can lead to a dramatic reduction in the number of offspring produced by a female over a lifetime. This is of great concern for wild species living under natural conditions.

Reproductive health of yellow perch Perca flavescens in selected tributaries of the Chesapeake Bay

“…A variety of environmental contaminants such as hepatochlor (Miller et al, 1999), dieldrin (Richardson et al, 2006), certain PCBs, organochlorine pesticides, metals and bisphenol A (Jones and Miller, 2008) have been shown to influence dopamine homeostasis in mammals and the hypothalamic-pituitary-gonadal axis in fishes (Khan and Thomas, 2006;Martyniuk et al, 2010;Page et al, 2011). Long-term dietary exposure of zebrafish to PCB mixtures mimicking environmental situations resulted in a decrease of maturing follicles and a reduction of fertilization rate (Daouk et al, 2011). In zebrafish, exposure to pentachlorophenol and methoxychlor inhibited oocyte maturation (Tokumoto et al, 2005).…”

Tribenuron methyl exposure inhibits oogenesis in zebrafish Danio rerio (Hamilton, 1822)

“…5) Sharma et al (2017) investigated effects of lead nitrate on Channa striatus ovaries and they detected severe histopathological changes in oocyte and connective tissue structure. Daouk et al (2011) observed decrease in the number of mature oocytes and an increase in the number of atretic oocytes in zebrafish ovaries after long-term exposure to polychlorinated biphenyls mixtures. They also noticed slight decrease in number of follicles at stage III (vitellogenic) and stage IV (mature oocyte), in comparison with control.…”

Effects of Aroclor 1254 on LH and 17,20β-P secretion in female Prussian carp (Carassius gibelio Bloch) in the spawning season

“…Polychlorinated biphenyls (PCBs) are lipophilic industrial chemicals that accumulate in living organisms (Okumura et al, 2003;Van Geest et al, 2011) and have negative physiological effects, mostly on the reproductive system of vertebrates, including fish (Khan and Thomas, 1997Gore et al, 2002;Coimbra et al, 2005;Gregoraszczuk et al, 2005;Coimbra and Reis-Henriques, 2007;Daouk et al, 2011). The impairment of reproduction in teleosts was found at a central level, at the hypothalamo-pituitary-gonadal axis, after the exposure to different PCB mixtures.…”

“…In females (Atlantic croaker, Nile tilapia, and zebrafish (Danio rerio)) exposed to PCBs, the observations include decreased ovary growth, the absence of maturing oocytes, and an increased number of atretic follicles Coimbra and Reis-Henriques, 2007;Daouk et al, 2011).…”

“…The aim of the present study was to evaluate the influence of Aroclor 1254 on the secretion of LH and 17,, which regulate the final stage of oocyte maturation in Prussian carp (Carassius gibelio B.). Because it is known that the alimentary tract is one of the most important contamination routes of PCBs in organisms (Daouk et al, 2011), we tested rectal administrations of PCBs (in addition to intraperitoneal injections) resulting in the high absorption of xenobiotics (de Boer et al, 1982).…”