Annals of Agricultural and Environmental Medicine 2014, Vol 21, No 4, 676–680

www.aaem.pl ORIGINAL ARTICLE

Reduction of Ochratoxin A in Chicken Feed

Using Probiotic
Katarzyna Śliżewska1, Małgorzata Piotrowska1
Institute of Fermentation Technology and Microbiology, Technical University of Lodz, Poland
1

Śliżewska K, Piotrowska M. Reduction of Ochratoxin A in Chicken Feed Using Probiotic. Ann Agric Environ Med. 2014; 21(4): 676–680.
doi:  10.5604/12321966.1129913

Abstract
Mycotoxins present in fodders may evoke health problems of animals and people. The data published by FAO in 2001
show that 25% of raw materials are contaminated with mycotoxins, while their type and concentration are to a great extent
dependable on the climatic zone. Biological detoxification of mycotoxins by the use of microorganisms is one of the well-
known strategies for the management of mycotoxins in foods and feeds. The aim of this study was to determine the influence
of spontaneous fermentation and that with the use of probiotic bacteria and yeast on ochratoxin A (OTA) concentration and
the microbiota pattern during fermentation. The probiotic preparation is a natural product containing bacteria resistant to
gastric juice and bile: Lactobacillus paracasei LOCK 0920, Lactobacillus brevis LOCK 0944, Lactobacillus plantarum LOCK 0945,
as well as live yeasts Saccharomyces cerevisiae LOCK 0140 of high fermenting capacity. After 6-hour fermentation with the
probiotic, in feed with a low concentration of ochratoxin A (1 mg/kg) the amount of ochratoxin A decreased by 73%. In the
case of high a concentration (5 mg/kg) the decrease in ochratoxin A was lower at about 55%. This tendency was sustained
during the following hours of incubation (12th and 24th hours). The application of probiotic bacteria and yeasts resulted in
the reduction of aerobic spore forming bacteria. It can be concluded that the probiotic preparation containing bacteria of
Lactobacillus strains and yeasts Saccharomyces cerevisiae used in the study was conducive to detoxification of ochratoxin
A added to a feed.
Key Words
ochratoxin A; detoxification; probiotic, feed

INTRODUCTION to be nephrotoxic, cytotoxic, carcinogenic, teratogenic and

immunosuppressive [7]. It may also induce gene mutation,
Ochratoxin A (OTA) is a contaminant often present in feeds although the mechanism of genotoxicity is not clear [8]. Oral
and foods of plant and animal origin. It is mainly produced LD50 values are 20 mg/kg for young rats and 3.6 mg/kg for
by several species of the genera Aspergillus and Penicillum chicks [9, 10].
[1]. This toxin can be formed during various phases of The course of acute ochratoksing is very rare, but cases
food production, already during the vegetation of plants of minor poisoning are very common (without noticeable
on the fields, during harvest and in storage. The ability to clinical symptoms), causing growth of body weight, laying,
synthesize mycotoxins is conditioned genetically, but it is bigger use of fodder and water, deficiency of vitamins A, C
also determined by environmental factors that include the and E, and reduced blood coagulability. The toxins attack the
following elements: substrate composition, its consistence, digestive and respiratory systems, kidneys, and liver, they
humidity, temperature and the presence of competitive damage the circulatory system, destroy digestive enzymes,
microflora [2]. cause allergies to food, and hamper the synthesis of proteins.
The data published by FAO in 2001 show that 25% of raw Ochratoxins also reduce immunity, which leads to higher
materials are contaminated with mycotoxins, while their susceptibility to colibacillosis and salmonellosis [11, 12].
type and concentration are to a great extent dependable on Biological detoxification of mycotoxins by the use of
the climatic zone. In spite of the fact that in Europe we can microorganisms is one of the well-known strategies for the
observe less favorable conditions for synthesis of mycotoxins management of mycotoxins in foods and feeds. Among the
than for instance in North America or Asia, the problem of different potentially decontaminating microorganisms,
the presence of mycotoxins in grains is also very important in Saccharomyces cerevisiae and lactic acid bacteria represent
numerous European countries (primarily the Scandinavian unique species which are widely used in food fermentation
countries, the southern parts of Germany, as well as Austria and preservation [13, 14].
and Italy) [3]. Therefore, contamination of animal feeds with The aim of this study was to determine the effeciency
mycotoxins is considered to be a world-wide problem [4, 5]. of a probiotic preparation composed of defined strains of
Several toxic effects of OTA have been described, such lactic acid bacteria, yeasts and a yucca extract in reduction
as inhibition of protein synthesis, impairment of calcium of ochratoxin A in chicken feed mixture during incubation
homeostasis, induction of lipid peroxidation, oxidative in vitro.
stress, and DNA damage, with species and tissue specific
differences [6]. Furthermore, this mycotoxin is considered
MATERIALS AND METHODS
Address for correspondence: Katarzyna Śliżewska, Institute of Fermentation
Technology and Microbiology, Technical University of Lodz, Wolczanska 171/173,
90-924 Lodz, Poland Materials. Wheat grain was inoculated with the strain of
E-mail: [email protected] Aspergillus ochraceus NRLL 3174 (Collection of Pure
Received: 19 November 2012; accepted: 11 June 2013 Cultures, Agriculture Research, Peoria, USA) and incubated
Annals of Agricultural and Environmental Medicine 2014, Vol 21, No 4 677
Katarzyna Śliżewska, Małgorzata Piotrowska. Reduction of Ochratoxin A in Chicken Feed Using Probiotic

to obtain high concentration of ochratoxin A in accordance immunoassay with horseradish peroxidase conjugate) using
with a procedure described by Xiao et  al. [15]. Twenty a commercial ELISA kits (OchraQuant Ochratoxin, Romer
Erlenmeyer flasks (500 mL), each containing 30 g of feed- Labs Diagnostic, Singapore) according to the procedure
grade wheat and 30 ml of distilled water, were autoclaved for described in the Ochra-Quant Assay kit manual. In brief:
30 min at 120° C and then inoculated with Aspergillus ochratoxin A was extracted from 10  g of sample with 50
ochraceus NRLL 3174. The culture was maintained at 30° C mL methanol:water (70:30 v/v). Independently, 100 µL
in a dark room. The fermentation was terminated on day 12 of conjugate mixture were added to each well containing
of incubation, the contaminated wheat was dried for 72 h, standards and previously filtered samples (50 µL). After
ground and the ochratoxin A concentration was determined. mixing, 50 µL were transferred to wells containing antibodies
The diet was formulated to meet or exceed the requirements and incubated for 15 min. Then, the content was eliminated,
of broilers (Table 1), adequate amount of contaminated wheat and the wells were washed five times with deionized water.
was substituted for uncontaminated one to obtain the final Any excess of water was discarded and the wells were dried.
concentration of 1 or 5 mg of ochratoxin A per kg of diet. Substrate (50 µL) was then added to each well, incubated
for 5 min, and the reaction was stopped by adding 50 µL
Table 1. Composition of the feed mixture for broiler chickens, g/kg1 stop solution. Optic density was read with an UVM 340
Component g/kg
microplate reader (Asys, Austria) using a 450 nm filter. The
ochratoxin A concentration was calculated by extrapolating
Wheat 330.7
the optic density with the respective calibration curve [17].
Soyabean meal 380.6
Maize 200.0 Microbiological Analyses. The microbiological analyses were
Limestone 8.5 carried out according to the Polish Standard of PN-ISO [18].
Dicalcium phosphate 18.0
The following bacteria species were identified: Lactobacillus
on MRS agar medium (Merck), using a double-layer technique
NaCl 3.0
and anaerobic incubation at 35° C/72 h; Clostridium on TSC
Rapeseed oil 50.0 agar (Merck) and anaerobic incubation at 37° C/18–24 h;
Vitamin-mineral premix 5.0 Pseudomonas on PM5 agar (BTL) and anaerobic incubation at
Wheat starch or probiotic 1.0 37° C/24 h; the coli group on VRBL agar (Merck) and aerobic
L-lysine (78%) 1.0
incubation at 35° C/24 h; total number of anaerobic bacteria
on Plate Count agar (Merck) and anaerobic incubation at
DL-methionine (98%) 1.2
35° C/24 h, and total number of yeasts on YGC agar (Merck)
Feed enzyme 1.0 and aerobic incubation at 20° C/120 h. Anaerobic bacteria
1
concentration of ochratoxin A in feed mixture was 1 mg/kg or 5 mg/kg were cultured in the anaerobic atmosphere of H:N:CO2 1:8:1
(Anaerobic Workstation Concept 400, Biotrace Int.). The
The probiotic preparation (PP) used contained (per specific morphology of cells was checked under a microscope
1 kg): 1010 of Lactobacillus cells (L. paracasei LOCK 0920, (Olympus CX-41). Each determination was done in triplicate.
L. brevis LOCK 0944 and L. plantarum LOCK 0945), 106 The results are presented as colony forming units (CFU) per
of yeast Saccharomyces cerevisiae LOCK 0140 cells and gram samples.
50 g of Yucca schidigera extract. The strains derived from
Centre of Industrial Microorganisms (LOCK), Institute Calculations and Statistical Analysis. Data were collected
of Fermentation Technology and Microbiology, Technical in triplicate subjected to tree-way analysis of variance by
University of Lodz in Poland. The strains were formerly used the general linear model (GLM) procedure of Statgraphics
in broiler trials [29], the preparation possess full probiotic Centurion XVI. Statistical significance was accepted at
documentation and is licensed [16]. P<0.05. In case when significant difference was found,
post-hoc Tukey HSD difference test was used to compare
Fermentation. The 1 kg samples of broiler diets with different between mean differences. For bacterial counts the analysis
ochratoxin A concentration were closed tightly in polyethylene of variance was carried out on data submitted to logarithmic
bags and sterilized by radiation with doses ranging 25 kGy at transformation.
ambient temperature. Radiation was carried out by 60Co γ-rays
at a dose rate of 0.2 Gy s-1, Fricke dosimetry being employed.
Sterilized control samples were kept tightly closed at 37°C RESULTS
and sampled after 6, 12 and 24 h for ochratoxin A analysis.
The one kg samples of each unsterilized diet without Fermentation With a Probiotic Preparation
supplement (spontaneous fermentation) or with addition After 6-hours of fermentation with the probiotic cultures, the
of 1 g PP per kg (probiotic fermentation) was mixed with amount of ochratoxin A was reduced to 0.45 mg/kg (by 55%)
distilled water in a proportion of 1:1.5 (w/w) and incubated in the case of the sample containing the initial concentration
at 37° C in an aerobic atmosphere for 24 h. Fermentation of ochratoxin A equal to 1 mg/kg in the medium, and to
was made in triplicate. After 6, 12 and 24 h of fermentation 1.36  mg/kg (by 73%) in the sample with a higher dose of
the 10 g of each diet were sampled for microbiological and the toxin. This reduction was sustained on the same level
ochratoxin A analysis. throughout the following hours of incubation. The results of
the analysis of variation in the ANOVA test showed that the
Analytical Procedures. The concentration of ochratoxin A probiotic preparation reduced the level of ochratoxin A in a
in wheat grain and in diets was measured with an enzyme statistically significant way in comparison with the sample
linked immunosorbent assay (ELISA direct competitive subject to spontaneous fermentation (Fig. 1).
678 Annals of Agricultural and Environmental Medicine 2014, Vol 21, No 4
Katarzyna Śliżewska, Małgorzata Piotrowska. Reduction of Ochratoxin A in Chicken Feed Using Probiotic

Spontaneous Fermentation orders of magnitude, in yests counts by 4 orders of magnitude

During spontaneous fermentation, we observed that in the diets supplemented with the probiotic preparation
after 6-hours of fermentation of feed for broiler chickens (interactions probiotic x time were highly significant).
containing ochratoxin A (with the initial concentration of 1 The inhibition of viable aerobic spore forming bacteria
or 5 mg/kg) the amount of the toxin was reduced to 0.79 and increased in unsupplemented diets and decreased in the
3.15 mg/kg, respectively, which translates into 21% and 37% diets supplemented with probiotic (interactions probiotic
(Figure 1). This tendency was sustained during the following x time were highly significant). Significant interaction
hours of incubation (12 and 24 hours). (P<0.05) was found also between initial dietary ochratoxin
A level and time of incubation for anaerobic spore forming
Control (Irradiated Feed) bacteria, their numbers decreased in the diet containing 1 mg
After 6-hours of incubation at the temperature of 37oC of a ochratoxin A after 6 h, than slightly increased, while in the
feed mix that had been previously subject to radiation diet containing 5 mg ochratoxin A it increased with time of
sterilization, the amount of ochratoxin A was reduced to incubation (Tab. 2).
0.81 mg/kg (by 19%) in the case of the sample containing the
initial concentration of ochratoxin A equal to 1 mg/kg in the Table 2. Main effects of supplementation with probiotic preparation,
medium, and to 4.23 mg/kg (by 15%) in the sample with a dietary ochratoxin A level and time of incubation on bacterial and yeasts
counts, log CFU/g diet
higher dose of the toxin. This reduction was sustained on
the same level throughout the following stages of Anaerobic
incubation (Fig. 1). Main effect
Total no of spore
Lactobacillus
Total no of
bacteria forming yeasts
bacteria
a) Ochratoxin A level (A)
* * *
1
1 mg/kg 7.62 3.02 6.44 4.92

0.8 5 mg/kg 7.55 3.32 6.27 4.82

SEM 0.341 0.418 0.246 0.210
0.6
Probiotic (P) supplement
Without probiotic 7.12 4.10 a 4.33 A 2.87 A
0.4
With probiotic 8.05 2.24 b
8.37 B
6.87 B
0.2 SEM 0.341 0.418 0.246 0.210
Time of incubation (T)
0
6h 12h 24h 0 6.62 A 3.26 4.93 A 3.72 A
feed after radiation 6h 7.35 B
3.08 6.08 B
4.52 B
feed after spontaneous fermentation
feed after probiotic fermentation 12 h 7.95 C 3.13 6.98 C 5.18 C
24 h 8.42 D
3.22 7.42 D
6.07 D
b) 5
* * * SEM 0.095 0.079 0.135 0.100
Interactions
4
AxP Ns Ns Ns Ns
3 AxT Ns 0.05 ns ns
PxT >0.001 >0.001 >0.001 >0.001
2
a,b, A,B
within columns, for each main effect, means with different superscript letters are
significantly different at: a,b, P <0.05; A,B P<0.01
1

0
6h 12h 24h
feed after radiation
feed after spontaneous fermentation
DISCUSSION
feed after probiotic fermentation
Protection against mycotoxin contamination of plant
Figure 1. Concentration of ochratoxin A [mg/kg] in the diet raw materials processed in the course of biotechnological
(values are means of 3 replicates ± SEM): procedures and designated as feed for animals is primarily
a) initial concentration 1 mg/kg
b) initial concentration 5 mg/kg focused on preventive actions. These actions include proper
Asterisks indicate significant differences (P < 0.05). conditions of cultivation, harvesting and storing of the crops
[19]. If the plant raw material happens to be contaminated
with mycotoxins it should be subject to detoxication. In
Change in the Microflora Pattern case of feeds, FAO accepts some methods of mycotoxin
Main effects of experimental treatments on bacteria and yeasts elimination that use chemical compounds and physical
number was shown in Table 2. Initial dietary ochratoxin processes, but they have to fulfill numerous requirements.
A did not affect bacteria and yeasts counts. Lactobacillus, The requirements include a condition saying that the feeds
total bacteria and yeasts counts increased (P<0.01) during have to preserve their nutritive and sensory values, as well as
incubation in diets without and with probiotic preparation. the physical properties of the product. Moreover, the process
However, the increase in bacterial counts was higher by 2 of detoxification has to be economically justified [20].
Annals of Agricultural and Environmental Medicine 2014, Vol 21, No 4 679
Katarzyna Śliżewska, Małgorzata Piotrowska. Reduction of Ochratoxin A in Chicken Feed Using Probiotic

Ochratoxin A detoxification strategies are classified carbohydrate moieties of the cell walls. Also the detoxification
depending on the type of treatment – physical, chemical or of heterocyclic aromatic amines was explained by this
microbiological – and their objective is to reduce or eliminate mechanism [35]. However, since a decrease in their toxic
the toxic effects of ochratoxin A by destroying, modifying or effects was also observed in the case of cytosolic preparations
absorbing this mycotoxin. The ideal detoxification method of LAB, it was hypothesized that other mechanisms (e.g.
would be easy to use and economical, and would not generate interactions with short chain fatty acids) might also play a
toxic compounds or alter other food quality parameters such role [36]. As mentioned above, ochratoxin A is removed far
as nutrient content [21]. Thus, first the effect of particular more efficiently by viable bacteria, which can be taken as
stages of processing on toxin reduction should be studied an indication that processes other than binding to the cell
[22]. Where this is impossible, other additional ways of walls are involved (e.g. metabolic conversion by the release of
treatment (physical, chemical or microbiological) should specific enzymes). However, the mechanisms which account
be considered [23]. for the detoxification are not yet understood. In this context,
Biological detoxification of mycotoxins in food, raw it is notable that it has been shown that ochratoxin A is
products, mixed protein feeds and also in human and detoxified by the representatives of the ruminal microflora
animal organisms is a novel and very promising method. via cleavage of the peptide bond, which leads to release of
Among the organisms that have been used in scientific phenylalanine [37].
research into mycotoxin elimination, one should enumerate: On the other hand, the research presented hereby showed
Acinetobacter calcoaceticus bacteria, Aspergillus, Alternaria, that a probiotic preparation containing both lactic acid
Botrytis, Cladosporium, Phaffia, Penicillum and Rhizopus bacteria (Lactobacillus paracasei LOCK 0920, Lactobacillus
moulds [24], lactic acid bacteria of the Lactobacillus strains brevis LOCK 0944, Lactobacillus plantarum LOCK 0945, in
[25] and Saccharomyces yeasts [26, 27]. Ŝtyriak et  al. [28] the dose of 1010/1 kg of the preparation) and Saccharomyces
examined 10 yeast strains of Saccharomyces, Kluyveromyces cerevisiae yeasts LOCK 0140 (106/1  kg of the preparation)
and Rhodotorula in respect of detoxification of ochratoxin A. was conducive to inactivation of ochratoxin A in a typical
It was proven that some yeast species of the Saccharomyces feed mix for chickens. After 6-hours of fermentation at a
strains were characterized with the highest capability of low concentration of ochratoxin A (1 mg/kg), the amount
ochratoxin biodegradation. Scott et al. [29] showed a decrease of ochratoxin A decreased by 55%. In the case of a high
in the amount of ochratoxin A of 21% in malt wort during the concentration (5 mg/kg), the reduction in ochratoxin A was
fermentation of Saccharomyces cerevisiae var. carlsbergensis lower and equaled about 73%. This tendency was sustained
yeast. Nevertheless, special interest should be paid to lactic also in the subsequent (12 and 24) hours of incubation.
acid bacteria due to their favorable influence on human It can be concluded that the probiotic preparation
organisms and the widespread use in the production of containing bacteria of Lactobacillus strains and yeasts
fermented food. These bacteria inhibit the growth of moulds Saccharomyces cerevisiae used in the study was conducive
as well as their production of mycotoxins [30]. Probiotics also to detoxification of ochratoxin A added to a feed mixture
increase the use of feeds by means of producing hydrolytic for chickens. The application of probiotic cultures of bacteria
enzymes [31]. Non-digestible carbohydrates (often described and yeasts also resulted in the reduction of aerobic spore
as non-starch polysaccharides) hamper the access of gastric forming bacteria.
juices to nutrients contained in the cells of plant feeds. They
are also characterized by the ability to bind substantial Acknowledgements
amounts of water. Young animals fed with feeds containing The study was supported by the Polish State Committee for
significant amounts of soluble non-digestible carbohydrates Scientific Research, grant no R12 028 01.
are subject to a decrease in their productivity indicators and
diarrhea. They also tend to suffer from deficiency of vitamins
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