Undernutrition combined with dietary mineral oil hastens depuration of stored dioxin and polychlorinated biphenyls in ewes. 1. Kinetics in blood, adipose tissue and faeces.

Lucille Rey-Cadilhac,Yannick Faulconnier,Sébastien Alcouffe,Pascal Faure,Philippe Marchand,Anne Ferlay,Sylvain Lerch,Stefan Jurjanz,Carole Delavaud,Catherine Jondreville,Bruno Le Bizec,Ronan Cariou

doi:10.1371/journal.pone.0230629

Abstract

Food safety crises involving persistent organic pollutants [POPs, e.g. dioxins, polychlorinated biphenyls (PCBs), organochlorine pesticides] lead to systematic slaughter of livestock to prevent their entry into the food chain. Therefore, there is a need to develop strategies to depurate livestock moderately contaminated with POPs in order to reduce such economic and social damages. This study aimed to test a POPs depuration strategy based on undernutrition (37% of energy requirements) combined with mineral oil (10% in total dry matter intake) in nine non-lactating ewes contaminated with 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and PCBs 126 and 153. In order to better understand the underlying mechanisms of the depuration process, POPs kinetics and body lipids dynamics were followed concomitantly over 57-day of depuration in POPs storage (adipose tissue, AT), central distribution (blood) and excretion (faeces) compartments. Faecal POPs concentrations in underfed and mineral oil supplemented ewes increased by 2.0 to 2.6-fold, but not proportionally to lipids concentration which increased by 6-fold, compared to the control ewes. Nonetheless, after 57 days of depuration in undernutrition and mineral oil supplementation, AT POPs concentrations were 1.5 to 1.6-fold higher while serum concentrations remained unchanged compared to the control ewes. This was concomitant with a decrease by 2.7-fold of the AT estimated lipids weight along the depuration period. This reduction of the volume of the storage compartment combined with the increase of POPs faecal excretion in underfed and mineral oil supplemented ewes led to a reduction by 1.5-fold of the PCB 126 AT burden, while no changes were observed for TCDD and PCB 153 burdens (vs. no change for PCB 126 and increases for TCDD and PCB 153 AT burdens in control ewes). The original approach of this study combining the fine description at once of POPs kinetic and of body lipids dynamic improved our understanding of POPs fate in the ruminant.

Highlights

Persistent Organic Pollutants (POPs) encompass several molecules defined in the Stockholm Convention list such as polychlorinated biphenyls (PCBs), organochlorine pesticides and dioxins (e.g. 2,3,7,8-tetrachlorodibenzo-p-dioxin or TCDD)
This study aimed to test a POPs depuration strategy based on undernutrition (37% of energy requirements) combined with mineral oil (10% in total dry matter intake) in nine non-lactating ewes contaminated with 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and PCBs 126 and 153
This was concomitant with a decrease by 2.7-fold of the AT estimated lipids weight along the depuration period. This reduction of the volume of the storage compartment combined with the increase of POPs faecal excretion in underfed and mineral oil supplemented ewes led to a reduction by 1.5-fold of the PCB 126 AT burden, while no changes were observed for TCDD and PCB 153 burdens

Summary

Introduction

Persistent Organic Pollutants (POPs) encompass several molecules defined in the Stockholm Convention list such as polychlorinated biphenyls (PCBs), organochlorine pesticides (e.g. hexachlorobenzene and mirex) and dioxins (e.g. 2,3,7,8-tetrachlorodibenzo-p-dioxin or TCDD). All POPs have several common properties, they are toxic to animals and humans, persistent in the environment and they bioaccumulate in animal tissues [1]. POPs bioaccumulate in fat-rich tissues and organs of animals and are transferred to fat-rich excreta. The consumption of fat-rich food products of animal origin (fish, meat, milk and eggs) is the main route of human exposure to several POPs [2]. Several food safety crises, involving accidental contaminations of livestock by POPs, occurred in past decades [3]. As POPs depuration process is extremely slow, the contaminated livestock animals and their food products are often disposed rather than saved.

Objectives

Methods

Results

Discussion

Conclusion