Transfer of zearalenone to the reproductive system of female rainbow
trout spawners: A potential risk for aquaculture and fish consumers?
Maciej Wo
zny
a, *
, Kazimierz Obremski
b
, Tomasz Zalewski
c
, Maren Mommens
d
,
Alicja Lakomiak
a
, Pawel Brzuzan
a
a
Department of Environmental Biotechnology, Faculty of Environmental Sciences, University of Warmia and Mazury in Olsztyn, ul. Sloneczna 45G, 10-709,
Olsztyn, Poland
b
Department of Veterinary Prevention and Feed Hygiene, Faculty of Veterinary Medicine, University of Warmia and Mazury in Olsztyn, ul. Oczapowskiego
13, 10-950, Olsztyn, Poland
c
Department of the Salmonid Research in Rutki, Inland Fisheries Institute in Olsztyn, Rutki, 83-330,
_
Zukowo, Poland
d
AquaGen AS, PO Box 1240, N-7462, Trondheim, Norway
article info
Article history:
Received 4 February 2017
Received in revised form
12 June 2017
Accepted 4 July 2017
Available online 5 July 2017
Keywords:
Carry over
Food safety
Glucuronides
Metabolism
Mycotoxins
Tissue distribution
abstract
To investigate whether ZEN transfers from the alimentary tract of fish to the somatic cells of ovaries or
the oocytes, mature females of rainbow trout were orally exposed to ZEN at a dose of 1 mg$kg
1
body
mass. At sampling times of 2, 6, 12, 24, 48, and 96 h, tissues of the fish (intestine, liver, ovaries, oocytes,
muscles, and plasma) were extracted to determine the concentration of ZEN and its metabolites using
immunoaffinity columns and HPLC-FLD. Our results confirm that ZEN is transferred from the alimentary
tract to the reproductive system of the fish, and indicate that the mycotoxin concentrates in the somatic
cells of the ovaries. Importantly, ZEN transferred to the fishes' oocytes and muscles only to a limited
extent. Our additional survey of fish hatcheries and local stores indicated only trace amounts of ZEN
residuals in the samples that were collected in Poland and Norway between 2013 and 2015, which
probably reflects good hygienic conditions for the feed used in these hatcheries. Furthermore, our results
indicate that the health risk from dietary intake of ZEN from fish roe is negligible. However, the potential
of ZEN to transfer to the fish ovaries may be of concern for aquaculture.
© 2017 Elsevier Ltd. All rights reserved.
1. Introduction
Zearalenone (ZEN) is a mycotoxin produced by some Fusarium
and Gibberella moulds that commonly occur in plant materials.
These moulds infect agricultural crops (mainly cereals), resulting in
worldwide ZEN contamination of foodstuffs for animals and
humans (Zinedine et al., 2007; Rodrigues and Chin, 2012). The most
prominent effect of ZEN toxicity is its ability to induce structural
disorders or dysfunction in the reproductive system of livestock
animals, i.e. pigs, cattle, and poultry (Zinedine et al., 2007;
Minervini and Aquila, 2008). ZEN mimics the action of natural
hormones (i.e. estrogens), which gives rise to a number of repro-
ductive disorders in exposed livestock mammals, including
decreased libido, anovulation, and infertility (Kuiper-Goodman
et al., 1987; Fink-Gremmels and Malekinejad, 2007; Metzler et al.,
2010).
The activity of ZEN has also been shown to affect fish repro-
duction. For example, water-borne exposure of zebrafish (Danio
rerio) to ZEN can reduce spawning frequency (Schwartz et al., 2010)
or induce transgenerational changes in fecundity (Schwartz et al.,
2013). Although experimental data on the toxicity of ZEN in fish
models are constantly increasing, the potential of this mycotoxin to
interfere with the reproductive system of economically important
fish has been incompletely evaluated (Manning, 2010; Anater et al.,
2016; Matejova et al., 2017).
In livestock animals (especially pigs), the toxicokinetics of ZEN
have been extensively studied. Once ingested, ZEN is rapidly
absorbed from the gut. Then, during the I phase of drug meta-
bolism, it is primarily metabolized in the intestine and liver to its
major metabolites a- and b-zearalenol (a- and b-ZEL) by hydrox-
ysteroid dehydrogenases (a- and b-HSD, respectively). In addition,
this conversion also takes place in other tissues, e.g. erythrocytes
(Chang and Lin, 1984), or ovarian granulosa cells (Malekinejad et al.,
2006). In the II phase, the reductive metabolites of ZEN produced in
* Corresponding author.
E-mail address: maciej.wozny@uwm.edu.pl (M. Wo zny).
Contents lists available at ScienceDirect
Food and Chemical Toxicology
journal homepage: www.elsevier.com/locate/foodchemtox
http://dx.doi.org/10.1016/j.fct.2017.07.010
0278-6915/© 2017 Elsevier Ltd. All rights reserved.
Food and Chemical Toxicology 107 (2017) 386e394