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REVIEW OF THE OCCURRENCE OF OCHRATOXIGENIC FUNGAL SPECIES

AND OCHRATOXIN A IN SOME AGRICULTURAL PRODUCTS1

Marija M. Škrinjara*, Slavica Vesković-Moračaninb, Nevena T. Blagojeva,

Vladislava M. Šošoa and Irena Z. Suturovića
a
University of Novi Sad, Faculty of Technology Novi Sad, Bulevar cara Lazara 1, Serbia
b
Institute of Meat Hygiene and Technology, Kaćanskog 13, Belgrade, Serbia

Ochratoxin A (OTA) is one of the most important and widespread fungal toxic meta-
bolites, which has been detected in our country for years in feed and food, mostly origi-
nated from plants. It is a very important contaminant of the plant food commodities in
nephropathic areas of the Balkan and Mediterranean countries, but also in other countri-
es in Europe and worldwide. This paper reviews the occurrence of OTA-producing fungi
and OTA in some agricultural products (fresh fruits, dried fruits, fruit juices and other
fruit products, vegetable products, wine, vinegar, cereals, mill products, etc.)

KEY WORDS: ochratoxigenic fungi, ochratoxin A, agricultural products, contamination

Ochratoxin A (OTA) is a pentaketide mycotoxin produced by several Aspergillus and

Penicillium species in different plant products such as cereals, coffee beans, cocoa beans,
nuts, beer, wine, spices, vine fruits (raisins, currants and sultanas) and other (1-6).
The majority of OTA-producing species from the Aspergillus genus belong to the
sections Circumdati and Nigri (Table 1; 3), and the majority of species from the Peni-
cillium genus that have been reported to produce OTA belong to the section Chrysogena
(Table 2; 4, 7).
OTA has been shown to possess carcinogenic (8), nephrotoxic (9), immunotoxic (10),
teratogenic (11) and genotoxic properties (12, 13).
OTA also has been implicated as the agent responsible for the Balkan Endemic
Nephropathy (BEN), a fatal kidney disease, primarily affecting rural populations in the
central Balkan Peninsula (14, 15).
The International Agency for Research on Cancer (IARC) has given OTA a Group 2B
classification – a possible human carcinogen (16).

* Corresponding author: Marija Škrinjar, Professor, University of Novi Sad, Faculty of Tehnology, Bulevar
Cara Lazara 1, 21000 Novi Sad, Serbia, e-mail: skrinjarm@uns.ac.rs
1
The paper was presented as invited lecture on the Microbiologia Balkanica, 7th Balkan Congress of Micro-
biology, October 25-29, 2011, Belgrade, Serbia

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Table 1. Species from the genus Aspergillus, producers of OTA (3)

Subgenus Section Species

Circumdati Circumdati melleus Yukawa
ochraceus K. Wilh.
ostianus Wehmer
sclerotiorum Huber
sulphureus (Fres.) Thom and Church
Flavi alliaceus Thom & Church
Nigri aculeatus (?)
awamori Nakaz. (?)
carbonarius (Bainier) Thom
foetidus Thom & Raper
japonicus Saito
tubiginensis Mosseray (?)
Wentii wentii Wehmer

Table 2. Species from genus the Penicillium, producers of OTA (4, 7)

Subgenus Section Series Species

Penicillium Chrysogena Chrysogena chrysogenum Thom
Verrucosa nordicum Dragodni&Cantoni
ex Ramírez
verrucosum Dierckx
Viridicata Camemberti commune Thom
Viridicata aurantiogriseum Dierckx
Group Series Species
Monoverticillata Frequentans purpurescens Sopp
Biverticillata Purpurogenum purpurogenum Stoll
- Symmetrica Rugulosum rugulosumThom

The OTA-producing moulds are widespread in fruits, fruits products, cereals and their
products in our country. Milić (16) and Škrinjar et al. (5, 17) established that A. awamori
and A. niger were found to be the most frequent among aspergilli isolated from oranges,
apples, peaches, hazelnuts, raisins and orange juice (Table 3).

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Table 3. Some OTA-producing Aspergillus species isolated from fruits and fruit products
in Serbia (5, 16, 17)

Species Fruits – fruit products

A.awamori Orange (healthy)
Orange (rotten)
Orange juice
Hazelnut
A.niger Apples
Orange
Orange juice
Peach
Hazelnut
Raisins
A.ochraceus Apples
A.sulphureus Orange
Orange juice
A.wentii Cherry juice

In the genus Penicillium, P. aurantiogriseum and P. chrysogenum were observed as

dominant contaminants of fruits and their products (bases, concentrate, and juice) (Table
4) (5, 6, 18).

Table 4. Some OTA-producing Penicillium species isolated from fruits and fruits
products in Serbia (5, 6, 18)

Species Fruits - fruit products

P. aurantiogriseum Orange – mango base
Orange base
Exotic base
Orange – pineapple base
Lemon base
Apple juice produced from concentrate
Apples
Orange (healthy)
Orange (rotten)
Orange juice
P. chrysogenum Lemon base
Orange base
Exotic base
Apples
P. commune Apple concentrate
Lemon base
Apple juice produced from concentrate
P.purpurogenum Orange
Orange juice

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A. niger and P. aurantiogriseum had a significant share in the mycopopulations isola-

ted from various frozen vegetables as well as from cereals and cereal products (19, 20).

Table 5. Some OTA-producing fungi isolated from frozen vegetables and cereals and
their products in Serbia (19, 20)

Species Product
A.niger Onion
Cauliflower
Carrot
Sweet corn
Wheat
Wheat flour
Barley
A. ochraceus Onion
P. aurantiogriseum Onion
Eggplant
Paprika
Cauliflower
Carrot
Corn
Corn flour
Wheat
Wheat flour
Barley

In many countries, special attention has been paid to OTA accumulation in fresh and
dried figs (21-25).
Doster et al. (24) and Bayman et al. (22), while investigating OTA production in figs
grown in California, established that about 40% of the fruits contained more than a trace
amount of OTA. Commercially cultivated figs that were naturally infected with Aspergil-
lus species Section Circumdati (A. alliaceus, A. melleus, A. ochraceus, A. sclerotiorum)
contained OTA at concentrations from zero to 9600.00 µg/kg (Table 6).
A high contamination of fresh and dried fruits with OTA-producing fungi and OTA is
often observed in Mediterranean regions. Zohri and Ardel-Gawad (26) studied OTA con-
tents in dried figs, apricots and plums in Egypt and found up to 120.00 µg/kg in dried
figs, 110.00 µg/kg in dried apricots and 280.00 µg/kg in dried plums. In Turkey, Özay
and Alperden (27) analyzed 103 fig samples and found only a 3% incidence of OTA
(5.20 – 8.30 µg/kg) (Table 6).
Table 6 gives OTA concentrations established in various fresh and dried fruits and
vegetables in different countries according to the literature data (17, 22, 24, 27, 28, 29).

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Table 6. OTA in fresh and dried fruits and vegetables (17, 22, 24, 27, 28, 29)

Fruits Max. (mean) OTA level (µg/kg)

California figs 9600.00
and vegetables
Fresh fruits

Cherries, Germany 27.10

Tomatoes, Germany 1.44
Strawberries, Germany 1.44
Apples, Germany 0.41
Figs, Turkey 8.30-337.00
Figs, Egypt 120.00
Apricots, Egypt 110.00
Plums, Egypt 280.00
Currants, UK 53.60
Sultanas, UK 20.00
Raisins, UK 18.10
Dried figs, UK >10.00
Figs, Switzerland 160.00
Raisins, Egypt 250.00
Dried fruits

Olives and olive oil, Morocco 40.00-80.00

Currants, Greece 12.40
Sultanas, Greece 4.85
Currants, Canada 4.85
Raisins, Canada 26.10
Sultanas, Canada 26.10
Vine fruits (black), Argentina 14.00
Vine fruits (white), Argentina 7.50
Raisins, Qatar 1.20
Black sultanas, Brazil 33.90
White sultanas, Brazil 5.00
Dates and plums, Brazil 5.00
Figs, Brazil 30.00
Raisins, Serbia 42.00
Raisins purchased in Hungary 6.20

The presence of mycotoxins can be also detected in the parts of fruit tissue where
fungal infection could not be observed. Engelhardt et al. (28), while studying OTA conta-
mination in several fruits after the removal of rotten tissue, established the toxin in cher-
ries at the levels up to 27.10 µg/kg and lower levels in tomatoes, strawberries, apples and
peaches (Table 7). These findings indicate the potential hazard in fruits intended for
consumption, even after the removal of rotten parts.

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Table 7. OTA concentration in fruits and vegetable after removal of rotten area according
to Engelhardt et al. (28)

Fruit, vegetable Maximum (mean) OTA level (µg/kg)

Apple 0.41
Cherry 2.71
Peach 0.59
Strawberry 1.44
Tomato 1.44

The occurrence of OTA in fruit juices and related products. OTA was also often
detected in fruit juices by numerous researches. According to Majerus et al. (30), low le-
vels of OTA were found in Germany in blackcurrant, tomato and carrot juices (Table 8).
Filali et al. (31) analyzed 14 samples of various fruit juices (orange, mango, pineapple,
clementine, grapefruit and peach juices) from Morocco. They found that the grapefruit
juice contained OTA at a concentration of 1160.00 ng/l, but no OTA was observed in the
other samples at the levels above the quantification limit of 0.01 µg/l.

Table 8. OTA in fruit juices, fruit pulp and musts according to Majerus et al. (30) and
Filali et al. (31)

Product Country Max. (mean) OTA level (ng/l)

Red grape juice Switzerland 311.00
Tomato juice Germany 32.00
Black currant juice Germany 60.00
Red grape juice Germany 5300.00
White grape juice Germany 1300.00
Grapefruit juice Morocco 1160.00
Pulp of frozen grape Brazil 35.40
Red grape juice Brazil 100.00
Red grape juice Canada and USA 104.00
White grape juice Canada and USA 71.00
Grape juices and drinks Poland 64.70
Grape juices Japan 6.00
French musts France 461.00
Spanish musts Spain 813.00
Tunisian musts Tunisia 4300.00

Occurrence of OTA in wines. There are a lot of data which reported the presence of
OTA in wines. Zimmerli and Dick (32) pointed out that the mycotoxin is produced after
the grape harvest, but prior to the alcoholic fermentation. Some researchers (33, 34) fo-
und that the production of OTA may take place in the vineyard, where several factors af-
fect fungal development and OTA accumulation. These factors include: a) climatic condi-
tions and latitude, b) contact between barriers and relevant mycotoxigenic fungi, c) wo-
unds or injuries that allow the fungus penetration into the fruit and predispose it to infec-

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tion, d) grape cultivation practices, including the use of fungicidal treatments and phyto-
sanitation, and e) the wine-making techniques, including the type of maceration and con-
ditions of fermentation (34, 35, 36, 37, 38, 39). Some data on the presence of OTA in wi-
nes are given in Table 9.

Table 9. OTA in wines according to various authors (33-39)

Wine Country Max. (mean) toxin level (ng/l)

Red wine Switzerland 388.00
Rosé wine Switzerland 123.00
White wine Switzerland 178.00
Red wine Germany 7000.00
Rosé wine Germany 2400.00
White wine Germany 1200.00
Red wine France 270.00
Rosé wine France 110.00
White wine France 20.00
Commercial red wine Italy 7630.00
Commercial rosé wine Italy 1150.00
Commercial white wine Italy 970.00
European red wine 603.00
European rosé wine 161.00
European white wine 267.00
Southern Italy red wine Italy 3177.00
Southern Italy dessert wine Italy 3856.00
Red wine Morocco 3240.00
Rosé wine Morocco 540.00
White wine Morocco 180.00
Mediterranean red wine 3400.00
Red wine Spain 316.00
White wine Spain 208.00
Northern Greece red wine Greece 2690.00
Northern Greece rosé wine Greece 1160.00
Northern Greece white wine Greece 1720.00
Dessert wine Greece 2820.00
South African red wine 380.00
South African white wine 300.00
Portuguese wine Portugal 2100.00
Red wine Brazil 42.40
Rosé wine Brazil 35.40
White wine Brazil 28.20
Red wine Argentina 42.40
Red wine Chile 70.70
Red wine Canada 393.00
White wine Canada 156.00
Red wine Poland 6710.00
White wine Serbia Traces

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Occurrence of OTA in vinegars. OTA was detected in vinegars, too. Majerus et al.
(30) pointed out the presence of this toxin in 50% of the wine vinegar samples analysed.
Its concentrations ranged from 10.00 to 1900.00 ng/l.

CONCLUSION

OTA is a toxic fungal metabolite ubiquitously found in different food commodities,

particularly agricultural products. Considering its very harmful effects to human and ani-
mal health, it is essential to monitor its presence in feed and food, especially in the areas
that has been classified as nephropathic, but on the other hand contamination with moulds
and with OTA can bring the big economic losses. In this area of the Balkan countries,
reports showed the high incidence of OTA in food and feed, so there is an increased risk
of health disorders caused by this agent. However, the presence of OTA has to be also
monitored in other European countries, especially in the Mediterranean basin, as well as
all around the world. This paper has pointed out the commodities that are the most fre-
quently contaminated with OTA-reducing fungi and with this mycotoxin.

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ПРЕГЛЕД НАЛАЗА ОХРАТОКСИГЕНИХ ПЛЕСНИ И ОХРАТОКСИНА А

НА НЕКИМ ПОЉОПРИВРЕДНИМ ПРОИЗВОДИМА

Марија М. Шкрињара, Славица Весковић-Морачанинб, Невена Т. Благојева,

Владислава М. Шошоа и Ирена З. Сутуровић
а
Универзитет у Новом Саду, Технолошки факултет, Булевар Цара Лазара 1, 21000 Нови Сад, Србија
б
Институт за хигијену и технологију меса, Каћанског 13, Београд, Србија

Охратоксин А (ОТА) је један од најзначајнијих и најраспрострањенијих ток-

сичних фунгалних метаболита, који се годинама детектује у нашој земљи, у храни
за животиње и у храни за људе, које су углавном биљног порекла. Изузетно је
важан контаминант хране биљног порекла и изазива нефропатију у балканским и
медитернаским земљама, али такође и у другим земљама Европе и света. Овај рад
пружа преглед присуства ОТА-продукујућих плесни и ОТА у неким пољопри-
вредним производима (свеже воће, суво воће, воћни сокови, други производи од
воћа, производи од поврћа, вино, сирће, житарице, млински производи, и др.)

Кључне речи: охратоксигене плесни, охратоксин А, пољопривредни производи,

контаминацијa

Received: 31 May 2013.

Accepted: 20 September 2013.

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