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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
