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ZEARALENONE AS A POTENTIAL ALLERGEN IN THE ALIMENTARY TRACT – A REVIEW* Maciej Gajęcki, Magdalena Gajęcka, Łukasz Zielonka, Ewa Jakimiuk, Kazimierz Obremski Division of Veterinary Prevention and Feed Hygiene, Department of Veterinary Public Health Protection, Faculty of Veterinary Medicine, University of Warmia and Mazury in Olsztyn, Olsztyn Key words: phytoestrogens, mould fungi, zearalenone, immunology, intestinal tract, allergy It is a common opinion that pathologic signs of allergy are connected with the prompt anaphylactic reaction. The knowledge about the so-called late reaction of the response to the allergen is less widespread. In the case of frequent or constant exposure to the allergen of late type, chronic inflammation and irreversible tissue damage appear. It may happen due to the intake of low doses of zearalenone in plant material. Zearalenone in the first period of its activity interferes in the processes of protein synthesis. On the other hand, the presence of environmental estrogens affects feminization of fish, birds and mammals. These xenobiotics, including zearalenone, probably take part in pathological conditions that occur as a result of autoimmunization and allergy. These dysfunctions and pathological conditions are in majority of cases noted more often in females than in males. They are often the primary cause of the induced diseases of the allergic origin like asthma, inflammation of nasal mucosa, skin inflammation and disturbances in the alimentary tract. In addition, environmental estrogens directly influence the immunological system or more probably they indirectly modulate this system through other tissues in order to change the model of cytokines. This study presents the thoughts over the hazards for human and animal health posed by environmental estrogens (especially zearalenone) even in the allergies. In humans the number of the results that would allow for any conclusion is minimal. In this situation in first, their influence on the immunological system in animals was considered. Then, the pathological effect of low doses of the xenobiotic on the immunological system was estimated. It would be recommended to take longer period into account focusing on the results of the possible autoimmunization or allergy.
POLISH JOURNAL OF FOOD AND NUTRITION SCIENCES
Pol. J. Food Nutr. Sci. 2006, Vol. 15/56 No 3, pp.
ZEARALENONE AS A POTENTIAL ALLERGEN IN THE ALIMENTARY TRACT
– A REVIEW*
Maciej Gajęcki, Magdalena Gajęcka, Łukasz Zielonka, Ewa Jakimiuk, Kazimierz Obremski
Division of Veterinary Prevention and Feed Hygiene, Department of Veterinary Public Health Protection, Faculty of
Veterinary Medicine, University of Warmia and Mazury in Olsztyn, Olsztyn
Key words: phytoestrogens, mould fungi, zearalenone, immunology, intestinal tract, allergy
It is a common opinion that pathologic signs of allergy are connected with the prompt anaphylactic reaction. The knowledge about the so-called
late reaction of the response to the allergen is less widespread. In the case of frequent or constant exposure to the allergen of late type, chronic inflam-
mation and irreversible tissue damage appear. It may happen due to the intake of low doses of zearalenone in plant material. Zearalenone in the first
period of its activity interferes in the processes of protein synthesis. On the other hand, the presence of environmental estrogens affects feminization
of fish, birds and mammals. These xenobiotics, including zearalenone, probably take part in pathological conditions that occur as a result of autoim-
munization and allergy. These dysfunctions and pathological conditions are in majority of cases noted more often in females than in males. They are
often the primary cause of the induced diseases of the allergic origin like asthma, inflammation of nasal mucosa, skin inflammation and disturbances
in the alimentary tract. In addition, environmental estrogens directly influence the immunological system or more probably they indirectly modulate
this system through other tissues in order to change the model of cytokines.
This study presents the thoughts over the hazards for human and animal health posed by environmental estrogens (especially zearalenone) even
in the allergies. In humans the number of the results that would allow for any conclusion is minimal. In this situation in first, their influence on the
immunological system in animals was considered. Then, the pathological effect of low doses of the xenobiotic on the immunological system was
estimated.
It would be recommended to take longer period into account focusing on the results of the possible autoimmunization or allergy.
INTRODUCTION
In the animal organism there are three systems that deter-
mine its homeostasis, namely nervous, endocrine and immu-
nological systems. The smallest disruption in any of them can
induce a disease with irreversible changes.
This study shows a preliminary analysis of the influ-
ence of zearalenone (environmental modulator of the endo-
crine system – EDs – endocrine disrupters) that is present in
plant materials, on the animal organism and especially on the
immune system [Gajęcki, 2002; Sweeney, 2002; Čonková et
al., 2003; Zwierzchowski et al., 2004; Laciaková et al., 2005].
IMMUNOLOGICAL HYPERSENSITIVITY OF ANIMALS
Along the evolution, the immunological system created
many specific mechanisms that are indispensable to eliminate
or neutralise environmental infectious, toxic and other agents
potentially harmful to the mammals. It has been noticed that
immunological reactions in secondary response are especially
effective and dynamic. At the same time, the immunological
mechanisms defending the integrity of the organism against
internal dangers have been created. The immunological
response can become intensive and improper in both forms.
The situation when the immunological response is “distort-
ed”, which in turn leads to destruction in tissues and disease
is referred to as “hypersensitivity” [Sicherer, 2002; Sicherer
& Leung, 2004].
At the beginning, when the term “allergy” was used it
was understood as the change in reactivity of the organ-
ism exposed to the antigen for the second time. With time,
“hypersensitivity” was used as a synonym of irregularity of
the immunological response that comes from the exposure to
the external agents [Jackson, 2003].
Current conditions of animal breeding in highly devel-
oped countries are totally different from those of phylogenic
development of their ancestors [Sweeney, 2002]. The changes
concern the prevalence of infectious diseases, therapy, expo-
sure to new microorganisms, diet, environmental pollution
and many others. There is no doubt that these changes are
the cause of the high prevalence of different atopies, especial-
ly in highly productive animals and pets.
Phylogeny development of animals persisted in the condi-
tions of the constant contact with parasites and exposure to
viral and bacterial agents. It was the so-called “immunologi-
cal training”. Nowadays, many cases of allergy are noticed in
the countries of highly developed animal breeding and farm-
ing. The reasons of these allergies cannot be defined, and
what is worse, recognised. It results from the improving con-
ditions of farming and the fact that contacts between ani-
Author’s address for correspondence:
2M. Gajęcki et al.
mals and microorganisms (not necessarily pathogenic) have
become limited. Moreover, the disease does not affect ani-
mals which do not develop the natural immunity because of
the massive prophylactic vaccinations [Bolhuis et al., 2003].
It results in dysfunction of some immune mechanisms (e.g.:
predominance of the activity of lymphocytes Th2 in compar-
ison with Th1), which together with unused defence ability
against multicellular parasites (based on mast cells, eosin-
ophils and IgE antibodies) leads to the increased incidence
of allergies. That way of thinking is in agreement with the
hygienic hypothesis that univocally explains the reasons of
allergy in young organisms [Jackson, 2003].
It seems that high exposure to allergens especially in
youth is a propitious factor of the incidence or development
of allergy. However, it cannot be excluded that the frequen-
cy of allergy incidence is also caused by factors different than
massive exposure to allergen. It can be influenced by the sea-
sonal factors like infections [Kuhn & Ghannoum, 2003], diet,
climatic changes and environmental pollution of different
origin [Ansar Ahmed et al., 1999].
Allergens are antigens that are able to evoke allergic reac-
tion, which is connected with their ability to induce humoral
response with participation of IgE antibodies [Foster et al.,
2003]. The majority of naturally occurring allergens (xenobi-
otics, pollens or other organic compounds) are globular pro-
teins of molecular weight ranging from10 to 40 kDa. Some
allergic proteins contain saccharides or their metabolites, e.g.:
glucoronic acid that is a product of glucose oxidation. They
are usually well soluble in water.
A separate group of allergens are haptens – chemical
compounds that evoke allergic reaction after binding to the
carrier, e.g.: serum protein. It is estimated that 10–20% of
allergies are side effects of drugs [Sicherer & Leung, 2004].
There are two major types of the immunological response
to allergen. It can be immediate/anaphylactic reaction or late
reaction. The first type occurs in several minutes after expo-
sure to allergen and it stops in one hour. Common opin-
ion joins signs of allergy with immediate/anaphylactic reac-
tion, which is connected with degranulation of mast cells and
direct influence of mediators. Late response to the allergen,
which is clinically very important in veterinary practice, is less
known. In the case of often or constant exposure to late aller-
gen, chronic inflammation and irreversible destruction occur
in tissues. It is noticed during long-lasting intake of small
doses of zearalenone introduced with plant material.
MOULD FUNGI AND THEIR METABOLITES
Mould fungi are eukaryotic organisms that do not have
chlorophyll. In majority they are parasites and many of their
species are saprophytic organisms. However, their pres-
ence on plant or animal material intended for feed or food
should be treated as the important risk factor for animals
and humans [Čonková et al., 2003]. Undesired health effects
in mammals depend on the degree of the pollution by only
mould fungi (proteins present on their surface and in spores)
and on the number of secondary metabolites (micotox-
ins) present in the ground [Kuhn & Ghannoum, 2003]. Our
knowledge concerning the presence of allergenic proteins in
tissues of mould fungi and micotoxins (carried in animal
organism by the protein carrier) evoking particular diseases
is poor at the moment [Jarvis & Miller, 2005]. We can pre-
dict pathological effects regarding the introduction of some
mould fungi and several micotoxins introduced separately
to the human or animal organism. The recognition of clini-
cal changes in acute intoxication is much more difficult and
mixed intoxications have not been recognised so far [Gajęcki
et al., 2005].
Micotoxins are a group of secondary mould metabolites,
mainly of Penicillium, Aspergillus and Fusarium genera [Moss,
1991], that can exhibit acute toxic actions [Cetin & Buller-
man, 2005]. Acute toxic effects are exceptional but long-last-
ing exposure to low concentrations of particular micotoxins
can induce chronic diseases, liver and kidneys neoplasm and
others, including allergies [Jarvis & Miller, 2005]. Some of
them display mutagenic (aflatoxins, fumonisins, ochratox-
in A, luteoscirin, T-2 toxin), teratogenic (ochratoxin A, pat-
ulin, aflatoxin B1, T-2 toxin) [Smith et al., 1995] and estro-
genic (zearalenone) action [Cavaliere et al., 2005; Jarvis &
Miller, 2005]. Some micotoxins interfere in the protein syn-
thesis and evoke skin hypersensitivity and necrotic lesions.
They (e.g.: zearalenone) even decrease the level of antibodies
[Atroshi et al., 2002; Gajęcka et al., 2004]. Other micotoxins
have neurotic effects and their low doses cause convulsions in
animals. Slightly increased doses of these micotoxins lead to
changes in the brain or even to death [Pitt, 2000].
As the chemical compounds, the micotoxins are enumer-
ated among the aromatic carbohydrates (sometimes to ali-
phatic carbohydrates) with a low molecular weight. It deter-
mines their resistance against environmental agents and a
lack or weak immunogenic features [Cavaliere et al., 2005;
Speijers & Speijers, 2004] that influence the system in a sup-
pressive way.
Some research [Chełmońska-Soyta et al., 2005] have
attempted to identify the site where the micotoxin or a group
of micotoxins incorporates in the life functions of a cell
as well as to characterise pathological changes in tissues
(organs and cells). Some of the micotoxins have a stimulating
factor [Cavaliere et al., 2005]. It should also be considered
that some micotoxins have a reverse effect, e.g.: they evoke
negative interaction like patulin that protects fats against oxi-
dation [Riley, 1998; Riley & Norred, 1996]. Multiple research
showed the suppressive effects of trichotecens towards the
immune system in animals [Pestka et al., 2005; Riley, 1998;
Zielonka et al., 2003, 2004]. The examples given in the lit-
erature show that kidneys [Braunberg et al., 1994] and liver
[Kuhn & Ghannoum, 2003; Obremski et al., 2005] are the
most susceptible to the action of the xenobiotics analysed.
However, general reactions in the form of oedema or aller-
gy may occur as well [Fischer & Dott, 2003; Jarvis & Mill-
er, 2005].
ENVIRONMENTAL ESTROGENS
According to Anser Ahmed [2000], there are two, among
many others, terms valid in endocrinology. The first assumes
that sex hormones cannot be treated as “reproduction hor-
mones”. They influence non-reproductive functions of many
tissues and especially of the immunological system. The sec-
ond assumes that estrogens are present in the organism not
only as natural or synthetic compounds but they have also
environmental origin. These substances (not necessarily pol-
3
Zearalenone as a potential allergen in the alimentary tract
lution) are referred to as “environmental estrogens”. Major-
ity of them is enumerated in the group the so-called “endo-
crine disrupters” (EDs). They are commonly found in the
environment, i.e. in soil, air, water and in food [Yurino et
al., 2004]. The examples of pollution (xenoestrogens) are:
plastic (bisphenol-A), detergents and surface-active sub-
stances (nonylphenol), pesticides (DDT, dieldrin), chemi-
cal compounds of industrial origin (polychlorinated biphe-
nyls) [Malinowska, 2001; Brevini et al., 2005]. Natural EDs
that occur in the environment are: phytoestrogens (genistein,
coumestrol) [Chełmońska-Soyta et al., 2005] and micoes-
trogens – products of mould fungi of Fusarium sp. genera
(zearalenone) [Gajęcki, 2002].
Ubiquitous presence of environmental estrogens should
make us consider that they can affect wild organisms, farm
animals, pets and humans in an uncontrolled way. According
to Polischuk et al. [1995], global access to these substances is
evident. It is proved by the presence of DDT (xenoestrogen)
in blood and fat of wild animals and humans in the region
of Arctic, which is free from industry. Some of these com-
pounds occur also in other groups of wild animals. Feminisa-
tion of fish, birds and mammals is the effect of their presence.
It causes decreased hatching in birds, fish, turtles and path-
ological lesions in the reproductive tract of alligators [Fry
& Tone, 1981; Chapin et al., 1997]. Our previous research
[Gajęcki, 2002] and that carried our by others on different
estrogenic compounds [de Jager et al., 1999] showed that
these compounds cause increased uterus mass, decreased
efficacy of mating, and decreased number of litters. They
also negatively affect development of the reproductive tract
and sexual behaviour. Numerous environmental estrogens
become the cause of the decreased efficacy of the action of
natural endogenic estrogens, e.g.17b-estradiol. Many of them
are chemically stable and accumulate in the organism (in fat).
They can reach high concentrations. These compounds are
released while losing weight; in addition they can reach foe-
tus organism during pregnancy and colostrums or milk. They
bind to (block) estrogen receptors and they, probably, cause
the transfer of a receptor-ligand complex from cytoplasm to
the nucleus and provoke synthesis of particular proteins. The
phenomenon of binding (blocking) of these environmental
chemical compounds to new estrogen receptors is possible
[Arcaro et al., 1999]. Environmental estrogens that simulate
natural hormones (mimicry) block and change the effect of
binding of the hormone to receptor. They can also change the
metabolism of natural estrogens [Soto et al., 1995; Withan-
age et al., 2001].
The correlation between the presence of environmen-
tal estrogens capable of modulating the endocrine system
(endocrine disrupters – EDs) [Sweeney, 2002; Teilamann
et al., 2002] and their potential negative effect on human
and animal organism is not univocal. However, the results
of the analysis carried out on wild and farm animals and
pets prompt to consider development of the methods used
to determine the harmfulness of substances modulating the
endocrine system [Ansar Ahmed, 2000]. The division of EDs
on those inducing reversible and irreversible pathological
changes in mammals should be considered as well.
The aim of this review is to show the problem of a dou-
ble action of EDs on the immunological system, which is
often noticed [Yurino et al., 2004]. Ample studies have shown
that hormones of the reproductive system influence the mor-
phology of thymus and other parts of the lymphatic system.
Administration of estrogens causes thymus involution [Ansar
Ahmed et al., 1999; Walker et al., 1999]. On the other hand,
the involution of thymus, especially in the postnatal period,
causes changes in the endocrine tissues of the ovary, testis
and thyroid gland. Estrogens regulate the synthesis of serum
and uterus immunoglobulins – IgM, IgA and IgG [Wira &
Sandoe, 1987; Makkonen et al., 2001; Gajęcka et al., 2004].
They also evoke an increase in the production of specific and
non-specific antibodies [Kurup et al., 2000]. From the bio-
chemical point of view and taking interactions into account
it can be concluded that both those forms are not clear. It is
likely that hormones and cytokines serve a very important
function in the transmission of information between the two
systems: the reproductive and the immune one [Krakows-
ki et al., 2004]. This, probably, strict co-operation assumes
that the influence of the environmental estrogens on the tis-
sues in the reproductive system can also affect the immuno-
logical system. It is still controversial, however, if this result is
produced by the direct or indirect action of the environmen-
tal estrogens. It should also be considered if the immunolog-
ical system is a real aim for all EDs or environmental estro-
gens in particular.
Estrogens are also likely to take part in pathological con-
ditions that occur as a result of autoimmunization or aller-
gy. Commonly, the majority of these pathological conditions
are noticed more often in female than in male [Chełmońska-
Soyta et al., 2005]. Hormones of the reproductive system
are often one of the primary causative agents of the aller-
gic conditions like asthma, inflammations of nose mucosa,
and skin inflammations in humans and animals [Stubner et
al., 1999].
It is very likely that the environmental estrogens trigger
particular changes in the immunological system directly or
indirectly regarding non-lymphatic tissue. They act through
non-estrogenic receptors that fulfil the role of mediators. In
addition, they modulate the immunological system in order to
change the model of cytokines through influencing this system
directly or – what is more probable – indirectly, by other tissues
[Ansar Ahmed et al., 1999; Krakowski et al., 2004].
The aim of this review was not to outline the results of
ample research proving these suggestions but to present some
thoughts over the dangers posed by environmental estrogens
(including zearalenone) to human and animal health, even in
the part of clinical immunology – allergies.
CLOSING REMARKS
Apart from the results obtained in wild, farm animals and
pets there is still a question regarding the safety of the pres-
ence or the impact of the environmental estrogens on the
immunological system of humans. In humans, the number
of the results that would allow for any conclusion is minimal.
Therefore, firstly research should be undertaken to deter-
mine the impact of non-environmental steroids on the immu-
nological system in animals. Next, it would be very important
to estimate the pathological effect of low doses of hormones
on the immunological system. Yet, they should be applied for
a longer period and attention should be paid to the results of
potential autoimmunization or allergy.
4M. Gajęcki et al.
ACKNOWLEDGEMENTS
The study was financed under a research grant of PBZ
KBN 097/P06/2003.
*The lecture was presented at the I. National Conference
Allergens and Compounds that Cause Food Intolerance and
that Occur in Plant Raw Materials and Food”, 27th – 28th June
2005, University of Warmia and Mazury, Olsztyn, Poland.
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ZEARALENON JAKO POTENCJALNY CZYNNIK ALERGIZUJĄCY W PRZEWODZIE
POKARMOWYM – ARTYKUŁ PRZEGLĄDOWY
Maciej Gajęcki, Magdalena Gajęcka, Łukasz Zielonka, Ewa Jakimiuk, Kazimierz Obremski
Zespół Profilaktyki Weterynaryjnej i Higieny Pasz, Katedra Weterynaryjnej Ochrony Zdrowia Publicznego, Wydział
Medycyny Weterynaryjnej, Uniwersytet Warmińsko-Mazurski w Olsztynie, Olsztyn
W powszechnej opinii objawy chorobowe alergii kojarzą się z reakcją natychmiastową, anafilaktyczną. O wiele słabsza
jest znajomość, tzw. reakcji późnej odpowiedzi na alergen. W razie częstego lub ciągłego narażenia na alergen typu późnego
dochodzi do przewlekłego stanu zapalnego i nieodwracalnego uszkodzenia tkanek, co może mieć miejsce w wyniku długotrwa-
łego pobierania np. małych dawek zearalenonu z materiałem roślinnym. Zearalenon w początkowym okresie swej aktywno-
ści ingeruje w procesy syntezy białek. Efektem działania estrogenów środowiskowych jest feminizacja ryb, ptaków i ssaków. Te
ksenobiotyki, a w tym prawdopodobnie i zearalenon, mają również swój udział w stanach patologicznych powstałych w wyni-
ku stanów autoimmunizacyjnych i alergicznych. W większości przypadków te niedyspozycje czy stany patologiczne spotyka
się częściej u samic niż u samców. Są często jedną z pierwotnych przyczyn wywoływania stanów chorobowych na tle alergicz-
nym jak astma, stany zapalne śluzówki nosa czy stany zapalne skóry oraz niedyspozycje przewodu pokarmowego. W dodatku,
estrogeny środowiskowe wpływając na układ immunologiczny w sposób bezpośredni, albo co jest bardziej prawdopodobne,
w sposób pośredni przez inne tkanki, modulują układ immunologiczny tak, by zmienić model cytokin.
W pracy przedstawiono przemyślenia na temat zagrożeń jakie mogą nieść estrogeny środowiskowe (w tym szczególnie
zearalenon) dla zdrowia ludzi i zwierząt z punktu widzenia reakcji alergicznych. W odniesieniu do ludzi liczba wyników z któ-
rych można byłoby jednoznacznie cokolwiek wnioskować, jest znikoma. W związku z tym w pierwszej kolejności należałoby
zająć się ich wpływem, na układ immunologiczny u zwierząt. W dalszej kolejności dobrze byłoby określić efekty patologiczne
małych dawek ksenobiotyku na układ immunologiczny, ale przez dłuższy czas, koncentrując uwagę na wynikach ewentualnej
autoimmunizacji czy alergii
... In pigs, chickens and mice, T-2 toxin induced necrotic changes in the intestinal epithelium and in jejunal and ileal crypts [48]. The transport of antigens from the intestinal lumen during inflammations and allergic reactions [49] is intensified by higher permeability of the intestinal barrier caused by epithelial damage and by enhanced phagocytosis/transcytosis of enterocytes. A similar scenario is observed when enterocytes are exposed to low doses of deoxynivalenol (DON), ochratoxin and patulin. ...
... In gilts exposed to various doses of ZEN over a period of 4 weeks, the mycotoxin caused mucosal inflammations as well as damage to the epithelium and mucosa, which is consistent with the results documenting ZEN's negative influence on intestinal defense [42]. The results of in vivo studies demonstrated that both low and high doses of ZEN could contribute to intestinal inflammations [148] and allergies [49]. ...
... The discussed changes in lymphocyte subpopulations were noted in peripheral blood [150]. Subclinical inflammation of the small intestine [21,22] and allergic reactions [22,49] were noted in analyses of blood samples collected from mesenteric blood vessels (article in press), a region where the presence of a chemotactic factor could be expected, and in sites characterized by changes in T cell subpopulations [25]. Double-positive T cells are transported from the blood stream to intestinal mucosa [151], which increases their volumetric density in tissues. ...
Article
Full-text available
This study demonstrates that low doses (somewhat above the No Observed Adverse Effect Level, NOAEL) of the mycoestrogen zearalenone (ZEN) and its metabolites display multispecificity towards various biological targets in gilts. The observed responses in gilts were surprising. The presence of ZEN and zearalenols (ZELs) did not evoke a response in the porcine gastrointestinal tract, which was attributed to dietary tolerance. Lymphocyte proliferation was intensified in jejunal mesenteric lymph nodes, and lymphocyte counts increased in the jejunal epithelium with time of exposure. In the distal digestive tract, fecal bacterial counts decreased, the activity of fecal bacterial enzymes and lactic acid bacteria increased, and cecal water was characterized by higher genotoxicity. The accompanying hyperestrogenism led to changes in mRNA activity of selected enzymes (cytochrome P450, hydroxysteroid dehydrogenases, nitric oxide synthases) and receptors (estrogen and progesterone receptors), and it stimulated post-translational modifications which play an important role in non-genomic mechanisms of signal transmission. Hyperestrogenism influences the regulation of the host’s steroid hormones (estron, estradiol and progesteron), it affects the virulence of bacterial genes encoding bacterial hydroxysteroid dehydrogenases (HSDs), and it participates in detoxification processes by slowing down intestinal activity, provoking energy deficits and promoting antiporter activity at the level of enterocytes. In most cases, hyperestrogenism fulfils all of the above roles. The results of this study indicate that low doses of ZEN alleviate inflammatory processes in the digestive system, in particular in the proximal and distal intestinal tract, and increase body weight gains in gilts.
... In the remaining experimental groups, the percentage of EOS was lower than in group C. This observation suggests that ZEN can exert allergizing effects, which was confirmed in our previous study [54]. The observed decrease in WBC counts in all groups during the experiment points to probable immune suppression (as a consequence of gilt maturation), but this trend was least pronounced in group ZEN5. ...
Article
Full-text available
The aim of this study was to determine whether low doses of zearalenone (ZEN) influence the carry-over of ZEN and its metabolites to the bone marrow microenvironment and, consequently, haematological parameters. Pre-pubertal gilts (with a body weight of up to 14.5 kg) were exposed to daily ZEN doses of 5 μg/kg BW (group ZEN5, n = 15), 10 μg/kg BW (group ZEN10, n = 15), 15 μg/kg BW (group ZEN15, n = 15), or were administered a placebo (group C, n = 15) throughout the entire experiment. Bone marrow was sampled on three dates (exposure dates 7, 21, and 42—after slaughter) and blood for haematological analyses was sampled on 10 dates. Significant differences in the analysed haematological parameters (WBC White Blood Cells, MONO—Monocytes, NEUT—Neutrophils, LYMPH—Lymphocytes, LUC—Large Unstained Cells, RBC—Red Blood Cells, HGB—Haemoglobin, HCT—Haematocrit, MCH—Mean Corpuscular Volume, MCHC—Mean Corpuscular Haemoglobin Concentrations, PLT—Platelet Count and MPV—Mean Platelet Volume) were observed between groups. The results of the experiment suggest that exposure to low ZEN doses triggered compensatory and adaptive mechanisms, stimulated the local immune system, promoted eryptosis, intensified mycotoxin biotransformation processes in the liver, and produced negative correlations between mycotoxin concentrations and selected haematological parameters.
... It is likely that hormones and cytokines have a very important function in the transmission of information between the two systems: the immune and the reproductive one (63)(64)(65). This coherent cooperation supposes that the influence of the environmental estrogens on the tissues in the reproductive system can affect also the immune system (66). Feeding mice with zearalenone alone in a dose of (40mg/kg) for fourteen days revealed lymphopenia, significant decreases in some immunoglobulin (IgG and IgM) levels, thymocyte sub-types (CD3 + , CD4 + and CD8 + ), NK-cells and pro-inflammatory cytokines suppression (67,68). ...
Article
Full-text available
Mycotoxicosis refers to the deleterious pathological effects of different types toxins produced by some worldwide distributing fungi. Mycotoxins, as secondary metabolites are affecting different organs and systems both in animal and human beings. Zeralenone (ZEA), the well-known estrogenic mycotoxins, is an immunotoxic agent. This macrocyclic beta-resorcyclic acid lactone, is mycotoxin procreated as a secondary metabolic byproduct by several types of Fusarium, encompassing F. roseum,F. culmorum, F. graminearum and different other types. Attributing to its potent estrogenic activity, ZEA has been incriminated as one of the major causes of female reproductive disorders. Thus, the purpose of the present review article is to appraise the pathophysiological consequences and sub sequent explore the progress in the research field of zearalenone immunotoxicities.
... It is likely that hormones and cytokines have a very important function in the transmission of information between the two systems: the immune and the reproductive one (63)(64)(65). This coherent cooperation supposes that the influence of the environmental estrogens on the tissues in the reproductive system can affect also the immune system (66). Feeding mice with zearalenone alone in a dose of (40mg/kg) for fourteen days revealed lymphopenia, significant decreases in some immunoglobulin (IgG and IgM) levels, thymocyte sub-types (CD3 + , CD4 + and CD8 + ), NK-cells and pro-inflammatory cytokines suppression (67,68). ...
Article
Full-text available
Mycotoxicosis refers to the deleterious pathological effects of different types of toxins produced by some worldwide distributing fungi. Mycotoxins, as secondary metabolites are affecting different organs and systems both in animals and human beings. Zearalenone (ZEA), the well-known estrogenic mycotoxins, is an immunotoxic agent. This macrocyclic beta-resorcyclic acid lactone is mycotoxin procreated as a secondary metabolic byproduct by several types of Fusarium, encompassing Fusarium roseum, Fusarium culmorum, Fusarium graminearum, and different other types. Attributing to its potent estrogenic activity, ZEA has been incriminated as one of the major causes of female reproductive disorders. Thus, the purpose of the present review article is to appraise the pathophysiological consequences and subsequent explore the progress in the research field of zearalenone immunotoxicities.
... Despite those benefits, microorganisms can also exert negative effects on animals [37]. Pathogens produce toxic metabolites and faecal enzymes which can promote the generation of carcinogenic substances [38,39]. In the literature, the influence of gut bacteria has been analysed mainly in the context of intestinal microflora's ability to remove mycotoxins. ...
Article
Full-text available
Zearalenone is a frequent contaminant of cereals and their by-products in regions with a temperate climate. This toxic molecule is produced naturally by Fusarium fungi in crops. The aim of this study was to determine the influence of low zearalenone doses (LOAEL, NOAEL and MABEL) on the intestinal microbiome of gilts on different days of exposure (days 7, 21 and 42). Intestinal contents were sampled from the duodenal cap, the third part of the duodenum, jejunum, caecum and the descending colon. The experiment was performed on 60 clinically healthy gilts with average BW of 14.5 ± 2 kg, divided into three experimental groups and a control group. Group ZEN5 animals were orally administered ZEN at 5 μg /kg BW, group ZEN10—10 μg ZEN/kg BW and group ZEN15—15 µg ZEN/kg BW. Five gilts from every group were euthanized on analytical dates 1, 2 and 3. Differences in the log values of microbial counts, mainly Escherichia coli and Enterococcus faecalis, were observed between the proximal and distal segments of the intestinal tract on different analytical dates as well as in the entire intestinal tract. Zearalenone affected the colony counts of intestinal microbiota rather than microbiome diversity, and its effect was greatest in groups ZEN10 and ZEN15. Microbial colony counts were similar in groups ZEN5 and C. In the analysed mycobiome, ZEN exerted a stimulatory effect on the log values of yeast and mould counts in all intestinal segments, in particular in the colon, and the greatest increase was noted on the first analytical date.
... In pigs, chickens and mice, T-2 toxin induced necrotic changes in the intestinal epithelium and in jejunal and ileal crypts (Wan et al., 2013). The transport of antigens from the intestinal lumen during inflammations and allergic reactions (Gajęcki et al., 2006;Pinton and Oswald, 2014) is intensified by higher permeability of the intestinal barrier resulting from epithelial damage and by enhanced phagocytosis/transcytosis of enterocytes. A similar mechanism is observed when enterocytes are exposed to low doses of DON, ochratoxin A and patulin. ...
Article
Most plant materials are contaminated with small doses of Fusarium mycotoxins and its modified forms that exert subclinical toxic effects on humans and animals. The aim of this study was to evaluate the carry-over of zearalenone and deoxynivalenol (pure parent compounds) to intestinal and liver tissues during 6 weeks of exposure to mycotoxins administered per os to gilts. The experiment was performed on 36 gilts with average body weight of 25 ± 2 kg, divided into 2 groups: an experimental group (group E, administered zearalenone at 40 μg/kg BW and deoxynivalenol at 12 μg/kg BW daily with feed) and a control group administered placebo. Tissue saturation with mycotoxins was analysed by liquid chromatography in samples collected at weekly intervals. Six gilts were euthanized in each week of the study. The conducted analyses revealed: (i) a non-uniform increase in zearalenone levels in the duodenum, jejunum, ascending colon and the liver; and (ii) an increase in deoxynivalenol levels, mainly in the ileum, caecum, ascending colon and the transverse colon, and a minor increase in the liver. The degree of tissue saturation was determined by the type of mycotoxin, but not by the time of exposure.
... The neutrophil: lymphocyte ratio (Fig. 25) suggests that during the experiment (weeks I, III and IV) and in the last weeks of exposure (week V), the immune system was more stimulated in group E, probably by nutritional (Etim et al., 2014b) rather than functional stress (Sutherland et al., 2008). The percentage of eosinophils (Fig. 3) in total WBC counts increased considerably relative to group C throughout the experiment, which indicates that the analyzed mycotoxins could cause allergic reactions (Gaję cki et al., 2006). The drop in WBC counts in both groups (Fig. 1) points to a decrease in immune activity, which was more gradual in group E. ...
Article
The aim of this study was to determine whether exposure to low doses of ZEN + DON induces changes in serum biochemical and hematological parameters in pre-pubertal gilts. In the evaluated groups, minor but statistically significant changes were noted in selected serum biochemical parameters, including glucose, total cholesterol, ALT, AST, AP, total bilirubin, Pin, Fe, K and Cl, and in hematological parameters, including WBC, eosinophils, basophils, monocytes, Ht, Hb, MCHC, HDW and PLT. A statistical analysis of the results revealed significant differences between groups in the values of WBC, eosinophils, basophils, Hb, Ht, PLT, glucose, ALT, AP, total bilirubin, Fe and K. Change trends were noted mainly in weeks II and V-VI. An analysis of the metabolic profile of pre-pubertal gilts exposed to ZEN + DON indicates that homeostasis and biotransformation of ZEN + DON can be toned down at the expense of the animals' energy reserves. Body weight gains were lower in group E, and BW gains were not observed in weeks II and VI. The activity levels of gilts decreased in the first weeks of exposure (I and II), but the drop was minimized by a compensatory effect, or in the last two weeks of exposure due to nutrient deficiency or insufficient supply of protein and energy with feed and feed additives, which decreased BW gains. Low doses of mycotoxins induce completely different changes in the metabolic test than higher doses. The above can probably be attributed to: (i) a negative compensatory effect, (ii) initiation of adaptive mechanisms and stimulation of the immune system, probably due to the allergizing properties of mycotoxins, (iii) excessive loss of energy and protein due to more effective feed utilization, or (iv) involvement in detoxification processes which leads to fatigue. Depending on the body's energy stores, the above processes tend to tone down the biotransformation of low doses of the examined mycotoxins but in the present study, the BW of gilts did not increase under exposure to a combination of ZEN + DON.
Article
The aim of the study was to examine whether the process of exposure to low doses of ZEN generates changes in the hematological and biochemical image of blood serum. During the experiment, pre-pubertal gilts (up to 25kg) were administered per os ZEN at a dose of 40μg/kg BW (Group E, n=18) or placebo (Group C, n=21) on a daily basis for 42days. Blood samples for investigation were collected seven times at intervals of one week. In the experimental groups, slight but statistically significant changes in the values of selected biochemical blood indices such as glucose, ALT, Pin, total protein and Fe, or in hematological indices such as RBC, MCV, PLT, WBC, basophils, eosinophils and monocytes were observed. Based on statistical analysis between the groups, differences in the values of WBC, basophils, peroxidase negative cells, Hb, Ht, MCV, HDW, glucose, ALT, AP, total protein, iron or potassium were found. In Group E, decreasing trends in the values of PLT and glucose, and increasing trends in the values of total protein, Pin, Na and Cl were found. The described situations occurred during the last three weeks of exposure. Low levels of exposure to ZEN lead to completely different changes in the metabolic profile than those resulting from higher doses of the toxin. The stimulatory effect of mycotoxins, observed in initial stages of exposure, is eliminated when the compensatory response and adaptive mechanisms are triggered, and due to excessive loss of energy, which may point to more efficient feed utilization and/or detoxification processes. The values of body weight gain obtained in Group E were monotonically higher in four out of the six investigated weeks of exposure. The above changes were accompanied by a decrease in glucose concentrations and higher total protein levels (a rising tendency), which could have affected the rate of body weight gain.
Article
Water samples collected randomly from animal farms and feed mills using process water have confirmed the presence of zearalenone (ZEA). ZEA is a mycotoxin (undesirable substance) produced by fungi of the genus Fusarium, showing estrogenic properties. It has a significant effect on the development of the male and female reproductive system and fertility in humans and animals. Previous research results indicate that long-term exposure to low doses of ZEA may lead to pathological states in humans and animals. In view of the above, regulatory standards for the maximum allowable ZEA concentrations in water should be established as soon as possible, since this mycotoxin poses serious health risks to humans and animals.
Article
The aim of the study was to assess bacteriolytic activity of lysozyme and serum amyloid A (SAA) level in sheep affected with zearalenone mycotoxicosis. Bacteriolytic activity of lysozyme, and serum amyloid A (SAA) level are both the elements of innate humoral immunity. Lysozyme bacteriolytic activity in serum was determined by diffusion-plate method with reference to Micrococcus luteus. SAA concentration was determined by the use of commercial ELISA kit (Phase Serum Amyloid A Assai TP802). The highest lysozyme bacteriolytic activity was observed in sheep with total rectal and intestinal mucosal membrane prolapse. Lysozyme concentration values in animals with partial rectal prolapse were significantly lower. In the control group, lysozyme concentration was low and within the range considered as physiologically normal. The highest levels of SAA, which ranged from 38.5 to 172 μg/mL, were detected in sheep in which the highest lysozyme bacteriolytic activity was noted. From the data obtained, it is undoubtful that changes in SAA level in affected sheep and control sheep are reliable indicators of zearalenone mycotoxicosis progress and termination. The highest levels of SAA were noted in animals, which had the total rectal and intestinal prolapse in course of zearalenone mycotoxicosis, and after returning the rectum to the normal position, mucosal membrane necrosis occurred, which resulted in perforation and peritoneum inflammation. The observed differences in SAA level forming range in particular animals from infected group are conditioned by the character of inflammation process and intensity in organs altered by the disease, which are principal factors inducing changes in its concentration. The level of this protein in serum reflects activation state of immunological system and could be one of the criterions in sheep health assessment.
Article
Full-text available
This study briefly describes the history of mycotoxins and gives a general overview of the most frequently detected mycotoxins. The discovery, chemical structure, producers, as well as the occurrence of mycotoxins have been discussed.
Article
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The main arguments, discussed by different international organizations, which confirm the significance of problems connected with the presence of zearalenone in animal feed materials and their influence on the safety of food materials are shown in this review article. The main world research trends focused on zearalenone, as undesirable substances, are also presented. A variety of Fusarium fungi produce a number of different mycotoxins, for example zearalenone. Is not true that Fusarium fungi are they the most prevalent toxin-producing fungi only in the northern temperate regions, are also commonly found on cereals grown in the temperate regions of America, Europe and Asia. Zearalenone have been shown to cause a variety of toxic effects in both experimental animals and livestock, and have also been suspected of causing toxicity in humans. Zearalenone is a stable compound, both during storage/milling and the processing/cooking of food, and it does not degrade at high temperatures. Studies of metabolism indicate that zearalenone is fairly rapidly absorbed following oral administration, with the formation of a- and b-zearalenol and a- and a-zearalanol, which are subsequently conjugated with glucuronic acid. This mycotoxin and some of these metabolites have been shown to competitively bind to estrogen receptors in a number of in vitro systems. Binding to specific receptors has been demonstrated in the uterus, mammary gland, liver and hypothalamus of different species. Additionaly alterations of immunological parameters were found at high zearalenone concentrations in vitro. Zearalenone causes alterations in the reproductive tract of laboratory animals and domestic animals. Various estrogenic effects such as decreased fertility, increased embryolethal resorptions, reduced litter size, changed weight of adrenal, thyroid and pituitary glands and change in serum levels of progesterone and estradiol have been observed, and teratogenic effects were found in pigs and sheep. It may be that the safety of zearalenone could be evaluated on the basis of the dose which had no hormonal effects in pigs, the most sensitive species, and a temporary Tolerable Daily Intake for zearalenone of 0.2 mg/kg of body weight, could be established.
Article
Full-text available
The aim of the study was to determine pathogenic factors and histopathology lesions in the internal organs of selected rabbits suspected of having Zearalenone intoxication. The study was carried out on three females and one ma|e of the hyplus line. The level of zearalenone (ZEA) and its metabolite a-zearalenole (a-ZOL) was analyzed in the blood and liver using the high performance liquid chromatography (HPLC) method. The results obtained confirmed the presenc e of ZEA in both the blood and liver. The histopathology pattern of the uterus and ovaries were characterized by enlarged uterine glands, softening, oedema in the tunica mucosa and destroyed granule layer of the ovarian fo|lic|es. The above lesions are characteristic for ZEA intoxication i.e. zearalenone mycotoxicosis. Moreoveł numerous retrogressive lesions were noted in the liver, spleen and kidneys. The results obtained confirmed that the disturbances noted in the reproductive system of the rabbits were caused by the intake offeed containing zearalenone.
Article
Full-text available
The signs that occur in pigs during deoxynivaleno|e (DO ) intoxications are strongly expressed in the form of vomiting and dysenteric diarrhoea, which in many ca§e§ leads to death. However, the subclinical form of deoxynivalenole micotoxicosis is the most frequent Óne and it is also very difficult to diagnose even for €xperienced cliniciansl Laboratory determination of the presence of this xenobiotic in animal blood seems to be the ideal solution for the problem, but determination of the level of this intoxication and its influence on the animal body still causes a great deal of difficulties. The aim of the studv was to,,determine the"level of deoxynivalenole in pig plasma after intoxication of low doses (0.2 and 0l4 mg/kg b.w.) of this xenobiotic. Basing on the obtained results it was stated that the level of micotoxin determined in blood p|asma goes dolvn sinusoidally along with decreasing amplitude. The highest concentration§ were stated in both experimental groups in the third'hour after the t0xin had been,applied. The level of DON in b|ood plasma decreases with time. The decrease is faster in the group where the dose was 0.2 mg/kg b.w. In the sixth hour after application the DON concentration did not go below 2.63 ng/ml. A high level of 5.30 ng/ml was sustained till the ninth hour in the group where a doubled dose,of DON was applied. Low:levels óf deox}nivalenole in the samples taken l8 h atter intoxication indicate how important it might be to establish a proper time of sample taking. It is also indicative of the great cffort of the body in eliminating the xenobiotic.
Chapter
One reason to study mechanisms of action of mycotoxins is to reveal the initial biochemical lesions leading to the progression of diseases associated with consumption of mycotoxin-contaminated foods and feeds. The focus of this chapter will be on recent research on biochemical and cellular mechanisms of action of selected mycotoxins. There have been prior and excellent reviews covering the mechanisms of toxicity and carcinogenicity of mycotoxins (Kiessling 1986; Betinaj 1989; Chu 1991; Ueno 1991; Coulombe 1993).
Article
Studies on the relationships of cytokines with a period of pre- and post-embryo implantation and their role in the development and maintenance of placenta and for the pathology of abortions have provided new and valuable data on the mechanisms of immune regulation of reproduction. Currently cytokines are regarded as a primary factor of communication between the cells of the uterus and the developing embryo. Various agents participate in the production of cytokines, including ovarian steroid hormones, semen plasma, bioactive lipids and proteins produced in the uterus. Therefore cytokines play a key role not only in the local immune response but also in the reconstruction of the uterus necessary for adaptation of the developing embryo.
Article
Polychlorinated biphenyls (PCBs) are ubiquitous environmental contaminants whose effects on biological systems depend on the number of and the positions of the chlorine substitutions. In the present study we examined the estrogenicity of the fully ortho-substituted PCB, 2,2',6,6'-tetrachlorobiphenyl (2,2',6,6'-TeCB). This PCB was chosen as the prototypical ortho-substituted PCB to test the hypothesis that ortho-substitution of a PCB with no para- or meta-chlorine-substitutions results in enhanced estrogenic activity. The results indicate that 2,2',6,6'-TeCB is estrogenic both in vitro, in the MCF-7 cell focus assay, and in vivo, in the rat uterotropic assay. The estrogenic activity elicited by the addition of 5 μM 2,2',6,6'-TeCB to the medium of MCF-7 cultures was inhibited by the estrogen receptor (ER) antagonist, LY156758, suggesting that 2,2',6,6'-TeCB or a metabolite is acting through an ER-dependent mechanism. Results from competitive binding assays using recombinant human (rh) ER indicate that 2,2',6,6'-TeCB does not bind rhERα or rhERβ. A metabolite of 2,2',6,6'-TeCB, 2,2',6,6'-tetrachloro-4-biphenylol (4-OH-2,6,2',6'-TCB), does bind rhERα and rhERβ and is also 10-fold more estrogenic than 2,2',6,6'-TeCB in the MCF-7 focus assay; however, this metabolite is not detected in the medium of MCF-7 cultures exposed to 2,2',6,6'-TeCB. Taken together, the results suggest that the estrogenicity observed in human breast cancer cells and the rat uterus may be due to 1) an undetected metabolite of 2,2',6,6'-TeCB binding to the ER, 2) 2,2',6,6'-TeCB binding directly to a novel form of the ER, or 3) an unknown mechanism involving the ER. J. Cell. Biochem. 72:94–102, 1999. © 1999 Wiley-Liss, Inc.
Article
Fusarial toxins are toxic metabolites produced mostly by toxigenic micromycetes of genus Fusarium. Dominant mycotoxins of this group include trichothecenes, moniliformin, zearalenone, and fumonisins. Recently, special attention has been paid to these toxins because of their harmful effects on both animals and humans. On the basis of the available literature, we review here the characteristics of major fusarial mycotoxins with an emphasis on their toxic effects on animals. The most important fusarial mycotoxins, their sources, and their pathology including clinical signs, necropsy findings, as well as changes in haematological, biochemical, and immunological indices, are addressed.
Article
Mycotoxins can have an impact on economics by causing losses in farm animals or giving rise to difficulties in their management, or by rendering a commodity unacceptable in national or international trade, because it does not conform with national criteria laid down for maximum tolerated levels of certain mycotoxins. The formation of mycotoxins in human food or animal feeds can occur as a result of postharvest sp materials badly stored, or preharvest as a result of invasion of a crop plant by a mycotoxigenic mould which may have a pathogenic or symbiotic relationship with the plant. There is at least one situation (facial eczema of sheep) in which a mycotoxin (sporidesmin) is produced in the field but on dead plant litter rather than in the living plant.Given sufficient economic resources there should be no problem in controlling the postharvest formation of mycotoxins in storage, but in tropical developing countries these resources may not be available and problems do still occur. The formation of mycotoxins in the field may be far more difficult to control and may require quite radical changes in agricultural practice.