Mycotoxins in Fruits, Fruit Juices, and Dried Fruits: Review

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1514

Journal of Food Protection, Vol. 66, No. 8, 2003, Pages 1514–1527


Copyright q, International Association for Food Protection

Review

Mycotoxins in Fruits, Fruit Juices, and Dried Fruits


S. DRUSCH 1* AND W. RAGAB 2

1Arbeitsgruppe für Lebensmittelqualität und -sicherheit, University of Kiel, Heinrich-Hecht-Platz 10, 24118 Kiel, Germany; and
2Department of Food Science and Technology, Assiut University, Egypt

MS 02-394: Received 5 November 2002/Accepted 13 February 2003

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ABSTRACT
This review gives an overview of the presence of mycotoxins in fruits. Although several mycotoxins occur in nature,
very few (a atoxins, ochratoxin A, patulin, Alternaria toxins) are regularly found in fruits. It has been shown that the presence
of fungi on fruits is not necessarily associated with mycotoxin contamination. The formation of mycotoxins depends more on
endogenous and environmental factors than fungal growth does. Mycotoxins may remain in fruits even when the fungal
mycelium has been removed. Depending on the fruit and the mycotoxin, the diffusion of mycotoxins into the sound tissues
of fruits may occur. The in uence of the selection and storage of fruits and the in uence of different processing steps involved
in the production of fruit juices and dried fruits on possible mycotoxin contamination is described. It is shown that the careful
selection, washing, and sorting of fruits is the most important factor in the reduction of mycotoxin contamination during the
production of fruit juices. The processing of fruits does not result in the complete removal of mycotoxins.

Mycotoxins are metabolites of Ž lamentous fungi that invasion during ripening, as the pH of the tissue increases,
have deleterious effects in animals and, in some circum- skin layers soften, soluble carbohydrates build up, and de-
stances, in humans (100). They include a very large, het- fense barriers weaken (87).
erogeneous group of substances, and correspondingly my- However, the growth of fungi is not necessarily asso-
cotoxigenic species can be found in all major taxonomic ciated with the formation of mycotoxins. Within a species,
groups. Mycotoxins exhibit properties of acute, subacute, the mycotoxigenic potential of a fungus largely depends on
and chronic toxicity in animals and/or humans, with some the strain of the fungus. Apart from the species and strain
mycotoxins also being carcinogenic, mutagenic, and tera- of the fungus, the physical and chemical composition of the
togenic. Moreover, mycotoxins cause a loss of viability in matrix and environmental factors play major roles in my-
plant seeds, reduce the quality and acceptability of all types cotoxin formation. The presence of fungi provides no as-
of products, and limit the storability and decrease the nu- surance of mycotoxin contamination, and because of the
tritional quality of foods. Therefore, mycotoxins are con- stability of mycotoxins, they may be present in food when
sidered an important worldwide problem in terms of public fungi are no longer present. Furthermore, a fungus may
health, agriculture, and economics (10, 12, 32, 51). produce different mycotoxins, and a mycotoxin may be pro-
It is unavoidable that human and animal foods and duced by several different fungi. The contamination of
feedstuffs will be universally exposed to fungal invasion fruits with mycotoxins has not only caused health hazards
from the planting of the crop through harvesting, transpor- but also resulted in economic losses, especially to exporting
tation, and storage, and even into the grocery store, restau- countries (98). This review represents an attempt to encom-
rant, and home, where the product will await Ž nal use by pass and incorporate the large body of work on mycotoxins
the consumer (31). A characteristic shared by most fruits is in fruits, fruit juices, and dried fruits for producers and
high acidity. The pHs of fruits range from 5.0 to ,2.5, and manufacturers of this important category of foods.
this pH range is considered the single most important factor
in determining the types of microorganisms that can spoil RELEVANT MYCOTOXINS AND
this class of food. While most species of bacteria are in- MYCOTOXIGENIC FUNGI
hibited by such high hydrogen ion concentrations, yeasts Although a large number of different mycotoxins exist,
and molds are more aciduric, and for many fungal genera only a few of them are regularly found in foods. The my-
or species these pH values are tolerable, if not optimum for cotoxins most commonly found in foods are a atoxins, och-
growth. It is because of acidity, therefore, that fungi are the ratoxin A, patulin, and mycotoxins produced by Fusarium
principal spoilage microorganisms for fruits and fruit prod- species. The latter group of mycotoxins are not covered in
ucts (106). Fruits become increasingly susceptible to fungal this review, since their occurrence is limited to grains and
seeds. Table 1 gives an overview of the mycotoxins covered
* Author for correspondence. Tel: 149-431-8802370; Fax: 149-431- in this review and the relevant mycotoxigenic fungi pro-
8805544; E-mail: sdrusch@foodtech.uni-kiel.de. ducing them.
J. Food Prot., Vol. 66, No. 8 MYCOTOXINS IN FRUIT PRODUCTS 1515

TABLE 1. Mycotoxins and fungal species occurring in fruits


Mycotoxin(s) Fungi producing mycotoxin References

A atoxins B1, B2, G1, Aspergillus chevallieri, A.  avo-furcatis, A.  avus, A.  avus var. columnaris, 7, 60, 104, 122
G2 A. niger, A. oryzae, A. parasiticus, A. repens, A. ruber, A. tamarii, A. wentii
Alternariol, alternariol Alternaria alternata, A. tenuissima, A. solani 43, 114
methyl ether, tenuazon-
ic acid
Ochratoxin A Aspergillus alliaceus, A. melleus, A. ostianus, A. petrakii, A. sclerotiorum, A. 2, 3, 47, 49, 84, 97
sulphureus, A. fumigatus, A. versicolor, A. carbonarius, A. niger, A. ochra-
ceus, Penicillium verrucosum
Patulin Penicillium claviforme, P. expansum, P. urticae, P. patulum, Aspergillus cla- 17, 55, 64, 92, 93
vatus, A. giganteus, Byssoclamys fulva, B. nivea, Alternaria alternata
Citrinin P. expansum 29, 124

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Trichothecin Trichthecium roseum 118

A atoxins are biologically active secondary metabo- azonic acid, and several altertoxins (108, 125). Alternaria
lites produced primarily by Aspergillus  avus and Asper- toxins have produced a variety of adverse effects, including
gillus parasiticus (57). They were Ž rst detected and char- anorexia, emesis, gastrointestinal hemorrhages, and con-
acterized in the 1960s (15) and have been found in many vulsions, in animals. Fetotoxic and teratogenic effects have
forms of human foods to date. A atoxin B1 and structurally also been described (121).
related compounds are of major concern with respect to
public health, mainly because of their potential as powerful MYCOTOXIN FORMATION IN INOCULATION
hepatotoxins and carcinogens in humans and their proven EXPERIMENTS
toxicity to animals, birds, and Ž sh (129). Table 2 gives an overview of the experimental evi-
Ochratoxin A was originally isolated from Aspergillus dence of the production of mycotoxins on fruits inoculated
ochraceus in 1965. Several different ochratoxins exist, but with mycotoxigenic species.
ochratoxin A is the most common. It is primarily a neph-
rotoxin, but teratogenic, immunosuppressive, and carcino- A atoxins. Most papers concerning a atoxin forma-
genic properties have also been ascribed to it. The Inter- tion on fruits refer to Ž gs or citrus fruits. The fungus A.
national Agency for Research on Cancer classiŽ ed ochra-  avus has been shown to be a reasonably vigorous pathogen
toxin A as a possible human carcinogen (1, 53). Several on ripe Ž g fruits. Fig fruits are very susceptible to infection
other Aspergillus species are also capable of producing och- by A.  avus conidia on the exterior fruit surfaces as well
ratoxin A. Penicillium verrucosum is the only known and as by conidia carried into the interior of the fruit by insects.
conŽ rmed Penicillium species that is able to produce och- Buchanan et al. (25) discussed the question whether A.  a-
ratoxin A (3). The contamination of foods with ochratoxin vus is a fruit pathogen on Ž gs (with infection, colonization,
in cool climates is usually caused by P. verrucosum, where- and a atoxin production occurring in the orchard) or a sap-
as the occurrence of ochratoxin in foods in warmer and rophyte colonizing on the dried product. These authors
tropical climates is associated with A. ochraceus. found that green Ž g fruits are resistant to invasion by A.
Another mycotoxin with relevance to human health is  avus but that as the fruits become Ž rm and ripe and soften
patulin. Patulin has a broad spectrum of toxicities, including they lose their resistance. Le Bars (56) reported that Ž g
carcinogenicity (34) and teratogenicity (29) in animals. fruits are a suitable medium for a atoxin production be-
Symptoms of experimental cases of patulin toxicosis in an- cause they contain high carbohydrate levels, and this prop-
imals are lung and brain edema; liver, spleen, and kidney erty is more favorable for toxin formation than for mold
damage; and toxicity to the immune system (62). For hu- growth. In another study on the a atoxigenic potential of
mans, nausea, gastrointestinal disturbances, and vomiting raw dried fruits, Ž gs were found to have a higher potential
have been reported. Patulin is produced by approximately than apricots, pineapples, or raisins (71).
60 species belonging to .30 genera of fungi (54). The most The experiments of Buchanan et al. (25) indicate that
important producer of patulin is the apple-rotting fungus the conidia of A.  avus are capable of penetrating fruit skin.
Penicillium expansum, and apple products may therefore Spores on the surfaces of ripe Ž g fruits were able to infect
contain patulin when rotten apples have been processed. and colonize the fruits, suggesting that the conidia of A.
These products are of toxicological concern, since they are  avus are capable of penetrating the fruit skin rather than
frequently consumed by infants and young children. The entering the fruit through a wound. However, there might
World Health Organization recommends a maximum pat- have been several alternative ways for a wound pathogen
ulin level of 50 mg/liter for apple juice (128). Apart from like A.  avus to enter fruit readily. Minute wounds might
apples, patulin is also of concern with regard to tomatoes, have been present in the fruit skin. The foraging of micro-
in which rotting is most frequently caused by Alternaria scopic animals, such as insects or mites, might have caused
alternata. Many strains of A. alternata also produce my- wounds that were not readily visible to the human eye.
cotoxins such as alternariol, alternariol methylether, tenu- Another possibility is that sufŽ cient fruit juice may have
1516 DRUSCH AND RAGAB J. Food Prot., Vol. 66, No. 8

TABLE 2. Mycotoxin production on experimentally infected fruits


Commodity Fungus Mycotoxin(s) Reference(s)

Oranges Aspergillus parasiticus A atoxins B1, B2, G1, G2 90


Oranges A.  avus A atoxin B1 123
Grapefruit juice, grapefruit peel A.  avus, A. parasiticus A atoxins B1, B2, G1, G2 7
Orange juice A.  avus A atoxin B1 18
Figs A.  avus A atoxins B1, B2, G1, G2 25
Tomatoes Alternaria alternata Alternariol, alternariol methyl ether 82
altenuene, altertoxin I, altertoxin II
Apples, strawberries, blueberries, A. alternata Alternariol, alternariol methyl ether 63, 121
grapes, mandarines
Apples, tomatoes, blueberries A. alternata, A. tenuissima, A. solani Tenuazonic acid, alternariol, alterna- 114
riol methyl ether (altenuene, al-

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tertoxin)
Oranges, lemons A. citrii Tenuazonic acid, alternariol, alterna- 115
riol methyl ether (altenuene, alter-
toxin I)
Apples, peaches, strawberries, — Patulin 40
greengage tomatoes, bananas,
melons
Cherries Aspergillus clavatus, Penicillium Patulin 64
claviforme, P. expansum, P. patu-
lum
Pears A. alternata, P. expansum, Saccha- Patulin 55
romyces vesicarium

been present on the fruit surface to permit some fungal Patulin. Apples are commonly used for inoculation ex-
colonization, an event often facilitating penetration. Rapid periments undertaken to investigate the formation of patulin
fungal colonization and a atoxin accumulation presumably on fruits. Early Ž ndings indicated that the presence of a
continued until fungal growth was stopped by a lack of patulin-producing species does not necessarily imply patu-
moisture in the dried fruits (25). In any case, a atoxins lin production. Factors like incubation temperature, lesion
constitute a problem that is already present in the orchard. size, and substrate play important roles (105). Hasan (44)
Firm, ripe fruits show little contamination when they are studied mycelial growth and patulin production over time
dried immediately (112). in apples inoculated with P. expansum. Patulin production
In contrast to the situation for Ž gs, A.  avus grows on increased when the mycelial growth reached the late phase,
oranges only after the peel has been partially deteriorated in which the energy source in the medium is nearly depleted
by other microorganisms, partly because of the antifungal and sufŽ cient intermediates have accumulated. The degra-
action of citrus oil against A.  avus (123). Furthermore, dation of patulin over time has been observed, and this
studies involving the inoculation of citrus fruits with As- degradation has been attributed to the action of chemicals
pergillus conŽ rm the importance of the carbohydrate con- like organic acids leaching from the vacuole and to the
mycelium of P. expansum itself (44). Other fungi, e.g., Pen-
tent of the substrate but also indicate that other endogenous
icillium patulum, have also been shown to produce patulin
factors in uence mold growth and a atoxin production. Be-
when cultured on apples (64). Peaches, apricots, strawber-
cause of its higher content of nitrogenous compounds and
ries, greengage, and pears are also suitable substrates for
carbohydrates, the grapefruit peel was found to be a better
patulin production (40, 55).
Aspergillus substrate than grapefruit juice (7). A atoxin
With regard to the safety of fruit products, e.g., when apples
concentrations produced by the same strains of A.  avus or are to be cleaned and trimmed for juice production, the
A. parasiticus were 5 to 10 times as high in grapefruit peel diffusion behavior of patulin in the fruit is of interest. In
as in grapefruit juice. Citric acid, a major constituent of apples, the diffusion of patulin is limited to a depth of up
grapefruit juice, does not support toxin formation by A. to 1 to 2 cm from the infected area (96, 119). Similar results
parasiticus (31). have been reported for sound pear tissues, in which patulin
A decrease in a atoxin production over time was ob- diffusion at up to 0.6 cm was observed (55). In contrast,
served for A.  avus grown on oranges and in orange juice for tomatoes, the mycotoxin penetrates the entire fruit (96).
(18, 123). A atoxins are degraded by the mycelium of A. For tomatoes, Rychlik and Schieberle (96) found 450 mg
 avus itself. The production of a atoxins is at its maximum of patulin per kg at a distance of 4 cm from the infected
when the biomass reaches its optimal value, and a atoxin tissue with an inoculum concentration of 52.9 mg of patulin
production rapidly declines after the mycelium starts to au- per kg. On the basis of the higher water content and the
tolyze (123). lower content of structure-forming polysaccharides in to-
J. Food Prot., Vol. 66, No. 8 MYCOTOXINS IN FRUIT PRODUCTS 1517

matoes than in apples, these authors deduced a higher dif- against mycotoxin formation. The production of Alternaria
fusion coefŽ cient for patulin in tomatoes than for patulin toxins was demonstrated for naturally infected intact apples
in apples. The mycotoxin may therefore also penetrate and tomatoes and for inoculated intact oranges and lemons
through other ‘‘low-viscous’’ foods like blueberries, grapes, (115). Tenuazonic acid was the mycotoxin that was pro-
and melons. duced most abundantly by Alternaria species on lemons (A.
Because of health concerns about synthetic fungicides, citrii) and on oranges and tomatoes (Alternaria spp.), while
the use of natural substances to control the growth of Pen- alternariol was the predominant mycotoxin for apples.
icillium species and subsequent patulin production has re- Overall, mycotoxin contents in lemons were lower than
cently been investigated. Patulin production was found to those in oranges.
be inhibited by 0.2% lemon oil, and the use of 0.05% lemon Another factor affecting the growth of Alternaria spe-
and 0.2% orange oil was found to result in a reduction of cies is competition between fungal genera during growth.
90% (44). Research has also focused on microorganisms For example, it was shown that on strawberries the growth
that may be used as biofungicides. The antifungal activity of Alternaria is inhibited by the presence of fast-growing

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of Bacillus subtilis against the growth of P. expansum has molds like Botrytis and Rhizopus. Therefore, Alternaria
recently been demonstrated (39). species as mycotoxin-producing molds on strawberries are
not of great concern (121).
Alternaria toxins. Alternaria molds are commonly in-
volved in the fungal spoilage of stored fruits. A key char- NATURAL OCCURRENCE OF MYCOTOXINS
acteristic of Alternaria spp. is their ability to grow at low ON FRUITS
temperatures. For this reason, they are particularly involved Mycotoxin formation subsequent to the experimental
in the spoilage of fruits during refrigerated storage. The cultivation of a fungus on fruit tissue does not necessarily
growth of A. alternata and the production of alternariol and indicate that a mycotoxin naturally occurs on a fruit. The
alternariol methyl ether in grapes were demonstrated by natural occurrence of mycotoxins also depends on environ-
Tournas and Stack (121). Fruits generally affected by Al- mental factors that determine the growth of fungi, the fun-
ternaria rot are apples, tomatoes, grapes, blueberries, gal spectrum on a fruit, and endogenous factors. According
peaches, cherries, and citrus fruits (115). Some species of to the review by Pitt and Hocking (87), defense mecha-
Alternaria are nonspeciŽ c, while the occurrence of others, nisms in fruit appear to be highly effective against a variety
such as Alternaria citrii and Alternaria solanaceous, is lim- of fungi; relatively few genera and species are able to in-
ited to certain fruits. Stinson et al. (114) reported the for- vade fruits. Some fungi are highly specialized pathogens,
mation of tenuazonic acid, alternariol, alternariol mono- attacking only one or two kinds of fruits, and others have
methylether altenuene, and altertoxin I on tomatoes and ap- a more general ability to invade fruit tissue.
ples after inoculation with known toxigenic Alternaria
strains. All species (Alternaria tenuis, A. alternata, Alter- A atoxins and ochratoxin A. Reports concerning af-
naria tenuissima, and Alternaria solani) and strains pro- latoxins on fruits are limited to fruits from regions with
duced tenuazonic acid, alternariol, and alternariol methyl relatively high temperatures, which favor the growth of af-
ether when cultivated on apple and tomato tissue, except latoxin-producing species like Ž gs, dates, and citrus fruits.
for A. alternata 938 and A. solani, which did not produce Natural contamination with a atoxins has been demonstrat-
any mycotoxins when cultivated on tomato tissue. Concen- ed for Ž gs and oranges as well as apples, but in some stud-
trations of tenuazonic acid were much higher when Alter- ies no contamination could be observed for Ž gs, peaches,
naria spp. were grown on tomatoes, while concentrations or dates. Concentrations of up to 78 mg of a atoxin G1 per
of the dibenzo-a-pyrone toxins alternariol and alternariol kg and up to 63 mg of a atoxin B1 per kg have been an-
methyl ether were higher when Alternaria spp. were cul- alyzed in Ž gs at different production stages (81). Özay et
tured on apples. The formation of altenuene and altertoxin al. (79) concluded from the results of studies on Ž gs at
I was limited to A. alternata strains. These results clearly different harvesting times that contamination with a atox-
show that the extent of toxin formation depends on the ins occurs only if environmental conditions like tempera-
substrate on which the fungus is cultivated. ture and humidity are favorable. A similar conclusion can
The inoculation of homogenized blueberry and tomato be drawn for ochratoxin A. For example, of six peaches
tissue with wild strains isolated from those fruits resulted with cleaved moldy stones, only one was found to contain
ochratoxin A (37). Engelhardt et al. (37) analyzed different
in the formation of considerable amounts of tenuazonic
fruits after the removal of rotten tissue and found up to
acid, alternariol, and alternariol methyl ether (114). In con-
2.71 mg of ochratoxin A per kg in cherries and up to 1.44
trast, Tournas and Stack (121) reported the failure of Alter-
mg/kg in tomatoes and strawberries. Peaches and apples
naria strains to produce alternariol and alternariol methyl
were also contaminated with ochratoxin A, but to a lesser
ether on blueberries. Two major differences between the
degree. The results obtained by these authors show that
two studies concern the Alternaria strains involved and the
damaged or moldy fruits can be contaminated with ochra-
pretreatments used for the fruits. In the Ž rst study, by Stin-
toxin A to a certain degree, even after the removal of the
son et al. (114), the fruits were mechanically broken and
rotten parts.
steam disinfected, and this process causes substantial
changes in the texture and composition of the fruit. How- Patulin. The occurrence patulin on bananas, pineap-
ever, the fruit’s integrity does not necessarily protect it ples, grapes, peaches, apricots, plums, and tomatoes was
1518 DRUSCH AND RAGAB J. Food Prot., Vol. 66, No. 8

TABLE 3. Natural occurrence of mycotoxins on fruits


No. of samples positive/
Reference Toxin(s) Commodity no. of samples analyzed Maximum concn.

90 A atoxin B1 Oranges 8/25 52 mg/kg


A atoxins B1, B2, G1, G2 120 m/kg
44 A atoxins B1, B2, G1, G2 Apples, brown lesions 30/30 350 mg/kg
Apples, remainders 0/30 —
81 A atoxin B1 Figs, different production stages 23/66 63.0 mg/kg
A atoxin B2 before processing 37.7 mg/kg
A atoxin G1 78.3 mg/kg
A atoxin G2 15.0 mg/kg
79 A atoxins B1, B2, G1, G2 Figs 0/12 —
89 A atoxins B1, B2, G1, G2 Dates 0/5 —

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66 Citrinin Apples 14/351 0.92 6 0.63 mg/kg
37 Ochratoxin A Tomatoa 6/11 1.44 mg/kg
Cherrya 6/6 2.71 mg/kg
Strawberrya 4/10 1.44 mg/kg
Applea 2/4 0.41 mg/kg
Apricota 0/2 —
Peacha 1/9 0.59 mg/kg
Nectarinea 0/5 —
81 Ochratoxin A Figs 1/19 7.5 mg/kg
79 Ochratoxin A Figs 0/12 —
37 Ochratoxin A Peaches 21/56 0.21 mg/kg
21 Patulin Rotten areas of apples 21/26 2–113.000 mg/kg
44 Patulin Apples, rotten areas 30/30 1,000 mg/kg
Apples, remainders 30/30 300 mg/kg
120 Patulin Apples — 5 mg/kg
9 Patulin Blueberries 1/12 21 mg/kg
Raspberries 0/10 —
Strawberries 0/10 —
Cherries 0/10 —
Lingon berries 1/2 265 mg/kg
Peaches 1/8 6 mg/kg
Plums 1/6 4 mg/kg
Black currants 0/6 —
14 Patulin Cherries 9/10 113 mg/kg
Strawberries 8/10 145 mg/kg
Raspberries 3/5 746 mg/kg
Black mulberries 7/10 157 mg/kg
White mulberries 4/6 426 mg/kg
115 Alternariol Tomatoes 6/19 5.3 mg/kg
Apples 7/8 59 mg/kg
127 Alternariol Apples 1/22 160 mg/kg
115 Alternariol methyl ether Tomatoes 6/19 0.8 mg/kg
Apples 8/8 2.3 mg/kg
227 Alternariol methyl ether Apples 1/22 250 mg/kg
115 Tenuazonic acid Tomatoes 11/19 139 mg/kg
Apples 8/8 0.5 mg/kg
107 Tenuazonic acid Tomatoes, moldy 73/142 70 mg/kg
a After removal of rotten area from fruit.

reported in early studies, but the authors of these reports in the lesions of apples (21), and no correlation between
did not present data on the incidence and concentration of the size of the lesion and the patulin concentration was
contamination (40, 120). Table 3 shows that patulin has found. Martins et al. (68) recently showed that there are
been quantiŽ ed in different stone fruits, berries, and straw- differences in incidences and levels of patulin contamina-
berries in other studies; for example, during storage at 158C tion for different apple varieties. Lovett et al. (65) reported
for 1 week, patulin was found to be detectable in blueber- that in naturally rotted apples, P. expansum is the predom-
ries at a maximum concentration of 1,000 mg/kg (9). Pat- inant patulin-producing fungus. Other fungi also produce
ulin occurs most frequently by far in brown rot lesions of the mycotoxin but are not as rapidly invasive. They may
apples. Up to 130 mg of patulin per kg has been detected be identiŽ ed as patulin producers only when they gain a
J. Food Prot., Vol. 66, No. 8 MYCOTOXINS IN FRUIT PRODUCTS 1519

competitive advantage. For grapes, a strong in uence of removal of rotten fruits and fruit parts prior to further pro-
vine variety on patulin occurrence was observed (8). Most cessing (44, 117). Up to 99% of patulin can be removed
samples of the variety Müller Thurgau were more frequent- from the product through the trimming of the fruits (65).
ly contaminated with patulin than most samples of the va- Another effective step in the reduction of patulin is the
riety Riesling. It therefore seems likely that vine variety washing of fruits. Acar et al. (5) demonstrated that 54% of
also in uences the occurrence of patulin in apples. High patulin could be removed from the product by high-pres-
levels of patulin contamination in apples have recently been sure water spraying. A combination of washing and the
reported in Turkey (14). removal of rotten and damaged apples resulted in a 10-fold
decrease in the initial patulin concentration (58).
Alternaria toxins. In addition to patulin, Alternaria After the washing and trimming of the fruits, juice is
toxins have also been detected in apples. According to the pressed and usually clariŽ ed, heated, and Ž lled. Some of
review by Scott (101), alternariol has also been detected in these processing steps signiŽ cantly contribute to a reduction
red currants, raspberries, strawberries, gooseberries, and in patulin levels in fruit juice, while others have little in-
blueberries. The storage of fruits may lead to a signiŽ cant

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 uence. Analysis of the juice, the Ž lter cake, the pellet after
increase in mycotoxin concentration. centrifugation, and the sediment showed that nearly half of
MYCOTOXINS IN FRUIT JUICE the patulin had already been removed during the pressing
of the apples (22). This removal was attributed to the bind-
For fruit juices, contamination with mycotoxins de- ing of the mycotoxin to solid substances during pressing.
pends largely on the fruit from which the juice is produced. The second most effective step for the removal of patulin
The contamination of juice with mycotoxins usually results is centrifugation, which accounts for a ;20% reduction in
from the use of poor-quality fruit. The spectrum of myco- patulin content. Centrifugation in combination with Ž ning
toxins occurring depends on the type of fruit. Table 4 gives or enzyme treatment resulted in a smaller reduction in pat-
an overview of types of juices, mycotoxins detected, and ulin content because of a decrease in solid particles.
the maximum concentrations of mycotoxins. For the preparation of a clear juice, clariŽ cation is re-
In several countries, including Switzerland, Sweden, quired. ClariŽ cation can be achieved by conventional meth-
Belgium, Norway, and Italy, a maximum allowable con- ods such as Ž ltration with gelatin and bentonite or by ul-
centration of 50 mg of patulin per kg of apple juice has traŽ ltration. For ultraŽ ltration, no Ž ltering aids are required.
been established. The U.S. Food and Drug Administration In terms of the removal of patulin, conventional clariŽ ca-
has also established an action level of 50 mg/kg on a single- tion is more effective than ultraŽ ltration (5). Conventional
strength basis for patulin in apple juice, apple juice con- clariŽ cation and ultraŽ ltration resulted in average patulin
centrates, and apple juice products in the United States. In reductions of 39 and 25%, respectively.
Germany, a maximum patulin limit of 25 mg/kg for apple Similar results were observed by Gökmen et al. (42).
juice and puree is being discussed. Most of the research on In their study, six different clariŽ cation processes were
patulin has therefore focused on its behavior during the compared with respect to the reduction of patulin levels in
production of apple products, which will be reviewed in the the juice. The processes compared included conventional
following section. clariŽ cation with gelatin, conventional clariŽ cation with
Selection and storage of fruits. As described by Sy- bentonite, conventional clariŽ cation with bentonite in com-
denham et al. (117), ripened fruits are required for juice bination with activated charcoal treatment, ultraŽ ltration,
production, and these fruits are normally stored at low tem- and ultraŽ ltration in combination with pre occulation with
peratures under modiŽ ed atmospheres. Storage at low tem- gelatin and bentonite, with an adsorbent resin, or with po-
peratures alone is not sufŽ cient to prevent mycotoxin for- lyvinylpolypyrrolidine. Conventional clariŽ cation with ac-
mation, and therefore additional measures, such as the dip- tivated charcoal treatment was found to be the most efŽ -
ping of apple fruits in 3% sodium hypochlorite, are rec- cient process, resulting in a patulin reduction of 40.9%.
ommended (44). The limited availability of warehouse Reductions achieved with the ultraŽ ltration process were
storage facilities may also lead to the open storage of fruits. always ,11% regardless of whether the process was com-
As was demonstrated by Sydenham et al. (117), patulin bined with other treatments. The adsorption kinetics of pat-
levels for fruits stored in the open for 15 or 33 days were ulin on activated carbon have been characterized as a phys-
signiŽ cantly higher than those for fruits stored in the open ical, endothermic process (72). The temperature depen-
for 7 days. The percentage of waste material (rotten and dence of the adsorption kinetics was described with the use
damaged fruits) removed during the sorting of the fruits of the Langmuir model.
was found to increase from 1.8% (on day 15) to 3.2% (on Additives used in raw juice also in uence the decrease
day 33). Patulin levels for the rotten fraction increased from in patulin levels. After depectinization, clariŽ cation, Ž ning,
1,120 to up to 6,235 mg/kg over time. On the basis of the and Ž ltration, patulin reductions of 25% for apple juice,
results obtained, these authors concluded that pressed juice 50% for apple juice with 500 mg of ascorbic acid per kg,
from apples subjected to storage in the open for .7 days and 42% for apple juice with 100 mg of sulfur dioxide per
may contain patulin at .50 mg/kg. kg were observed by Aytac and Acar (17). In the same
study, no patulin reduction occurred during concentration
Processing. As shown in different studies, a key step and pasteurization. However, more severe heat treatment
in the prevention of the occurrence of patulin in juice is the leads to a degradation of patulin. The heating of apple juice
1520 DRUSCH AND RAGAB J. Food Prot., Vol. 66, No. 8

TABLE 4. Mycotoxins in fruit juices


No. of samples
positive/no. of
Reference Commodity Toxin(s) samples analyzed Maximum concn

4 Apple juice A atoxins B1, G1 5/5 30 mg/liter


Guava juice 2/5 12 mg/liter
67 Grape juice, white Ochratoxin A 21/27 1.3 mg/liter
Grape juice, red 56/64 5.3 mg/liter
Apple juice 0/33 —
Orange juice 0/30 —
Black currant juice 3/19 0.06 mg/liter
Tomato juice 3/30 0.032 mg/liter
132 Grape juice, red Ochratoxin A 7/8 0.311 mg/liter
Grape juice, white 0/3 —

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Apple juice 0/2 —
Orange juice 0/6 —
97 Grape must Ochratoxin A 8/11 0.461 mg/liter
38 Grapefruit juice Ochratoxin A 1/14 1.16 mg/liter
8 Grape must Patulin 30/64 230 mg/liter
21 Apple juice, conventional Patulin — 3.03 mg/kg
Apple juice, organic — 28.2 mg/kg
Apple juice with pulp — 1,150 mg/kg
28 Apple and mixed fruit juice Patulin 101/241 1,130 mg/liter
54 Baby juice Patulin 0/9 —
Juice drink 0/11 —
Pure apple juice 59/71 39.9 mg/liter
Mixed juice 0/14 —
95 Apple juice Patulin 10/10 26.0 mg/liter
Apple-acerola juice 1/1 0.7 mg/liter
Grape juice 2/2 5.2 mg/liter
Sour cherry juice 1/1 0.2 mg/liter
Blackcurrant juice 1/1 0.1 mg/liter
Orange juice 1/1 0.1 mg/liter
109 Patulin Apple juice 9/9 19.8 mg/liter
Pear juice 0/2 —
58 Patulin Apple juice 8/31 45 mg/liter
202 Patulin Apple juice 42/106 200 mg/liter
Black currant juice 3/10 200 mg/liter
Cherry must 1/5 200 mg/liter
6 Patulin Fruit juices (positive samples of apple, 8/44 60 mg/liter
pineapple, passion fruit juice)
41 Patulin Apple juice concentrate, diluted 215/215 376 mg/liter
8 Patulin Grape must 21/55 230 mg/liter
59 Patulin Quince juice 0/8 —
Apple juice 0/10 —
Pear juice 0/2 —
36 Patulin Apple juice and products 73/91 402 mg/kg
Pear juice 34 1–20 mg/kg
69 Patulin Orange juice 0/27 —
Grapefruit juice 0/19 —
Pineapple juice 0/21 —
Apple juice 0/17 —
Pear juice 0/16 —
Grape juice, red 0/12 —
Grape juice, white 0/8 —
70 Patulin Apple juice, from concentrate 39/101 30 mg/liter
Apple juice, directly produced 110/199 171 mg/liter
131 Patulin Apple juice 27/45 733 mg/liter
33 Alternariol Apple juice concentrate 17/32 5.42 mg/liter
Alternariol methyl ether 17/32 1.71 mg/liter
127 Alternariol, alternariol methyl Apple products 0/18 —
ether, altenuen, altertoxin I Tomato products 0/10 —
Other fruit products (pears, grapes, red 0/12 —
currants, strawberries, cherries, plums,
peaches, oranges, grapefruits)
Mixed fruit products 0/7 —
J. Food Prot., Vol. 66, No. 8 MYCOTOXINS IN FRUIT PRODUCTS 1521

for nearly 3 h at 1008C resulted in a patulin reduction of a atoxins remain in the peel, up to 13% remain in the pulp,
33% (52). and only up to 35% appear in the clear juice. Pasteurization
As can be seen from Table 4, the occurrence of och- did reduce a atoxin levels in juice by 9 to 20% for the
ratoxin A was limited to grape juice, especially red grape single toxins, and sterilization at 1008C for 30 min de-
juice. Zimmerli and Dick (132) suggested that ochratoxin creased a atoxin levels by up to 73%. The strongest heat
A in wines from southern European regions results from resistance was observed for a atoxin B1, and the next
the growth of mold after the grapes have been harvested. strongest heat resistance was observed for a atoxin G1.
The climatic conditions in these regions are not favorable Storage of the product at 25 to 358C for 20 weeks resulted
for the growth of ochratoxin A–producing fungi. Majerus in an 87% reduction in a atoxin B1 and a 100% reduction
et al. (67) pointed out that long-time enzymatic treatment in a atoxin G1.
of crude juice and berries at increased temperatures to im- In an early investigation of Alternaria toxins in fruit
prove the color of red grape juices and red wine favors juices, no contamination was detected in any of the samples
fungal growth and ochratoxin production. In contrast to pat- tested (127). It seems likely that the detection limit of the

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ulin, ochratoxin A remained stable during alcoholic fer- method used (which ranged, e.g., from 10 to 100 mg/kg,
mentation (132). depending on the fruit matrix, for alternariol) was not suf-
Ž cient. Scott (101) reported that alternariol has been de-
Stability in juice. In 1968, Scott and Somers (102) tected in apple juice, raspberry drink, grape juice, cranberry
observed that within 3 weeks of storage, initial concentra- juice, raspberry juice, and prune nectar. Alternariol methyl
tions of patulin decreased to 25, 75, and 65% in canned ether has been detected in apple juice and prune nectar.
orange, apple, and grape juices, respectively. These authors Alternariol and alternariol methyl ether were shown to be
concluded that these decreases during storage could be at- stable in apple juice with and without vitamin C over 20
tributed to the levels of sulfhydryl groups present in the days and at 808C after 20 min. Altertoxin I was found to
juices. Ascorbic acid present in the samples probably con- be moderately stable (101).
tributed to patulin degradation. Different studies in which
ascorbic acid has been added to apple juice or buffer so- MYCOTOXINS IN DRIED FRUITS
lutions clearly show increased patulin reductions in the Most investigations involving dried fruits deal with
presence of ascorbic acid (17, 24, 110). This reaction is fruits grown in warm climates, such as Ž gs, dates, and
believed to involve a metal-catalyzed oxidation of ascorbate grapes. The available data are very contradictory, indicating
or ascorbic acid (24). Free radicals are generated from this that many different factors affect fungal growth on and my-
reaction and may attack the conjugated double bond of the cotoxin contamination of such fruits.
patulin. Experimental evidence for this reaction is still lack- Zohri and Abdel-Gawad (133) analyzed samples of
ing. The addition of sulfur dioxide also leads to a reduction dried Ž gs, apricots, plums, and raisins for the natural oc-
in patulin levels in juices, although this effect is not as currence of a atoxins, citrinin, ochratoxins, patulin, ster-
pronounced as it is with ascorbic acid. For sulfur dioxide, igmatosyctin, diacetoxyscirpenol, T-2 toxin, and zearale-
a reversible binding and an irreversible binding of patulin, none. Only ochratoxin A was detected in all samples of
depending on pH, have been described (110). apricots (50 to 110 mg/kg), Ž gs (60 to 120 mg/kg), and
In general, the detected levels of patulin contamination plums (210 to 280 mg/kg) tested. All raisin samples were
of fruit juices presented in Table 4 are low, re ecting high- free of mycotoxins. MacDonald et al. (66) determined lev-
quality products and the use of good quality assurance and els of ochratoxin A and a atoxins in 60 samples of retail
management systems in the production chain. A high in- dried vine fruits purchased in the United Kingdom. Och-
cidence of patulin contamination has recently been reported ratoxin A concentrations exceeded 0.2 mg/kg in 19 of 20
by a Turkish research group (131). The incidence of apple currant samples, in 17 of 20 sultana samples, and in 17 of
juice contamination at levels of .50 mg/liter was 44%, and 20 raisin samples, with an overall incidence of 88%. The
the maximum concentration detected was 733 mg/liter. maximum level detected was 53.6 mg of ochratoxin A per
These results indicate that poor-quality fruits may have kg; no contamination with a atoxins was observed. Differ-
been used for these products, and this conclusion is rein- ences in the contamination levels found in these two studies
forced by the patulin results presented above for fresh may be due to different detection limits for the methods
fruits. used. Herry and Lemetayer (48) detected a atoxin B1 at
Another point that needs further investigation is Beretta low levels in 2 of 28 date samples and in 1 of 52 raisin
et al.’s (21) Ž nding that patulin levels are signiŽ cantly high- samples.
er in apple juice made from organic apples than in apple Youssef et al. (130) examined 100 dried-raisin samples
juice made from conventionally farmed apples. These au- of for mycotoxin contamination. A atoxin B1 was detected
thors conclude that the use of fungicides in conventional in two of these samples at concentrations of 300 and 220
farming may be responsible for the lower levels of myco- mg/kg, and ochratoxin A was found in one sample at 250
toxin contamination. mg/kg. Ragab et al. (89) analyzed 40 samples of dates and
The natural occurrence of a atoxins in orange juice has date products for a atoxin contamination. Two of Ž ve sam-
been described (4). Ragab (88) investigated the fate of af- ples of pitted date fruits stuffed with peanuts contained af-
latoxins in oranges inoculated with A. parasiticus during latoxin B1 at concentrations of 4.8 and 6.2 mg/kg. These
processing. This author showed that up to 69% of the single authors attributed the presence of a atoxin to previous con-
1522 DRUSCH AND RAGAB J. Food Prot., Vol. 66, No. 8

TABLE 5. Occurrence of mycotoxins in dried Ž gs The occurrence of a atoxins is not necessarily associ-
Mycotoxin(s) Frequencya Concn Reference ated with visible changes in fruit. From a batch of 160 kg
of dried Ž gs, 386 Ž gs (8.6 kg) were randomly taken and
Total a atoxins 1/187 10 mg/kg 12 analyzed individually for a atoxin contamination by Stein-
6/67 14 mg/kg 12 er et al. (112). A atoxins B1 and G1 were found in 94 and
1/8 19 mg/kg 12 49 Ž gs, respectively, at concentrations of 0.2 to 30 ng/g.
— 150–241 mg/kg 94 To determine whether the a atoxin contamination was as-
24.0% 10–165 mg/kg 103
sociated with the dark-colored Ž gs, 16 dark, discolored Ž gs
9.0% .100 mg/kg 103
35
were sorted out and analyzed individually by the same in-
32/83 325 mg/kg
8/42 126 vestigators. Only eight of these Ž gs contained a atoxin B1,
A atoxin B1 1/350 .100 mg/kg 91 and three of them also contained a atoxin G1.
1/140 .100 mg/kg 91 In a different study, Steiner et al. (111) analyzed dried
94/386 0.2–30 mg/kg 113 Ž gs showing bright greenish yellow  uorescence under UV

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8/16 0.2–20 mg/kg 113 light for the presence of a atoxins, cyclopiazonic acid, ko-
6.4% 112 mg/kg 23 jic acid, and ochratoxin A. BGY  uorescence is not emitted
2/4 11.8 mg/kg 45 by the a atoxin itself but by kojic acid, a compound pro-
6/54 124 mg/kg 99 duced by A.  avus at the same time a atoxin is produced.
8/15 1.9 mg/kg 48 This  uorescence is commonly used in the food industry
37/52 5–76 mg/kg 111
as a screening device for the detection of a atoxins. The
8/42 260 mg/kg 126
23
removal of BGY- uorescent Ž gs from a 56-kg batch effec-
A atoxin B2 6.4% 51 mg/kg
2/54 27 mg/kg 99 tively lowered the contamination level from 22.6 to 0.3 mg
A atoxin G1 49/386 0.2–30 mg/kg 113 of a atoxin B1 per kg. All 52 BGY-positive Ž gs contained
3/16 0.2–5 mg/kg 113 kojic acid at concentrations of 8 to 6,900 mg/kg. Thirty-
6.4% 61 mg/kg 23 seven (71%) fruits were contaminated with a atoxin B1 at
2/54 345 mg/kg 99 concentrations of 5 mg/kg and 76 mg/kg, and 15 (29%)
15/52 5–180 mg/kg 111 fruits contained a atoxin G1 at levels of 5 mg/kg to 180
A atoxin G2 2/54 59 mg/kg 99 mg/kg. Ochratoxin A concentrations ranging from 5 mg/kg
Ochratoxin A 12/52 5–12 mg/kg 111 to 12 mg/kg were detected in 12 (23%) fruits at cone. These
11/54 185 mg/kg 99 results demonstrate that dried Ž gs exhibiting BGY  uores-
4/4 60–120 mg/kg 133
cence are likely to be contaminated with mycotoxins.
— Traces–6,900 mg/kg 35
0.1% 370–7,860 mg/kg 20 Factors involved in the high contamination levels
Kojic acid 52/52 8.0–6,900 mg/kg 111 for dried fruits. It is evident from Table 5 that dried Ž gs
a are a high-risk commodity among dried fruits. Incidence of
Number of samples positive/number of samples analyzed or per-
centage of samples positive. contamination for a fruit is presumably in uenced by fac-
tors such as the suitability of the fruit as a substrate and
the frequency of infection of the fruit with toxigenic molds
(as discussed above), as well as harvesting and drying con-
tamination of the peanut kernels with which the date fruits
ditions and moisture content or water activity (aw ) value.
had been stuffed. Head et al. (46) reported that copra con-
tained ,20 mg of a atoxin B1 per kg. Both a atoxin and Harvesting and drying conditions. The traditional
free fatty acid contents increased with increasing degrees method applied for the harvesting and drying of Ž gs in
of contamination with A.  avus. Turkey was described by Özay and Alperden (81) as fol-
As can be seen from Table 5, several investigations on lows. The ripe Ž gs are left on the trees until they shrivel.
mycotoxin contamination in Ž gs have been conducted. As The Ž gs fall to the ground and are gathered up and dried
is the case for other dried fruits, a few contaminated Ž gs further in the sunlight on a drying device. This sun-drying
may result in the contamination of a whole batch of fruits. process takes almost 5 days. After drying, the sound fruits
Özay and Alperden (81) examined 103 samples collected are sorted out from the damaged ones and stored in farm
from various orchards and at various stages of Ž g process- storehouses. Obviously, the environmental conditions as-
ing, including samples of dried Ž gs and Ž g paste produced sociated with these procedures seem favorable for myco-
from these dried Ž gs. Overall, a atoxins B1, B2, G1, and toxin production in infected fruits. Anton (13) reported that
G2 were present in 29% of the samples examined at levels the temperature in the Ž g cultivation regions during the
of 0.5 to 63.0 mg/kg, 0.5 to 37.7 mg/kg, 0.5 to 78.3 mg/kg, ripening, harvesting, and drying of the fruits ranged from
and 0.5 to 12.5 mg/kg, respectively. Ochratoxin A was de- 27 to 308C, which is close to the optimum temperature for
tected in only 3% of the samples at levels of 5.2 to 8.3 mg/ mold growth and mycotoxin formation. Generally, if the
kg. In samples collected during the sun drying of Ž gs, only moisture content of the stored crop exceeds 13 to 18%,
a atoxin B1 and G1 were detected. In the Ž g paste, after mycotoxin formation can occur (27). As is the case for
the dried fruits had been homogenized, all a atoxins and mycotoxigenic fungi and their toxins in grains and seeds,
ochratoxin A were found at concentrations lower than those critical points in the formation of mycotoxins in dried Ž gs
in Ž gs at previous production stages. during storage are moisture content, storage conditions,
J. Food Prot., Vol. 66, No. 8 MYCOTOXINS IN FRUIT PRODUCTS 1523

TABLE 6. Minimum aw values for the growth and mycotoxin for- fungal growth occurred at aw values of 0.85 to 0.88 (76,
mation of some potentially toxic molds (16, 19, 27, 73–78, 81, 83, 77). Pitt and Miscamble (83) studied the effects of water
86) activity in combination with temperature on the growth of
Minimum aw value for: some molds. These authors found that the minimum aw val-
ues for the germination and growth of A.  avus, Aspergillus
Mold Fungal growth Mycotoxin formation oryzae, and A. parasiticus are very close to 0.82, 0.81, and
Aspergillus  avus 0.78–0.82 0.83–0.87 0.80, respectively, at 52, 30, and 378C, respectively. Mean-
A. parasiticus 0.80–0.82 0.83 while, for Aspergillus nomius, the minimum aw value for
A. ochraceus 0.77 0.88 germination and growth is a little higher, i.e., 0.83 at both
A. nomius 0.81–0.83 — 25 and 308C but 0.81 at 378C.
A. versicolor 0.80 — Dried Ž g fruits stored in farm storehouses are quite safe
Penicillium 0.82 0.90 in terms of their moisture contents and aw values. It can be
P. viridicatum — 0.90 concluded that the contamination of dried Ž gs with myco-
P. expansum 0.83–0.85 0.99

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toxins can start on the tree and can continue in the bulk
P. patulinum 0.83–0.85 0.95 during storage as a result of poor drying and of storage
P. clavatus 0.83–0.85 0.99
conditions such as high temperatures and relative humidi-
P. citrinum 0.84 —
ties, as well as the rewetting of dried fruits.
Prevention and control of contamination of dried
and, with respect to the analysis, heterogeneous distribution fruits. Because of the variety of factors in uencing my-
within a lot of fruits. Dried Ž gs are comparable large fruits, cotoxin contamination, such contamination is usually not
and therefore the moisture content within a fruit and within associated with one production stage, but one stage may be
a lot may vary. Moistened parts offer the opportunity for more important than the others depending on the crop, the
fungal growth with subsequent accumulation of mycotoxins fungus, the mycotoxin, and the environmental conditions.
and water resulting from the respiratory activity of the Mycotoxin contamination of dried fruits may start with fun-
molds. So-called hot spots with very high a atoxin con- gal contamination on the trees, increase during harvesting
centrations can develop in stored fruits (81). Steiner et al. and sun drying, and continue to accumulate during storage
(113) investigated the distribution of a atoxins in an a a- because of rewetting and improper conditions.
toxin-contaminated lot of Ž gs and found concentrations of Swanson (116) demonstrated that environmental stress
0.4 to 37.0 mg/kg in different sublots. These results show conditions such as insect infestation, drought, cultivar sus-
that very few highly contaminated Ž gs may lead to a sig- ceptibility, mechanical damage, nutritional deŽ ciencies, and
niŽ cant concentration of a atoxins in an entire lot. unseasonable temperature, rainfall, or humidity can pro-
Özay et al. (79) studied the in uence of harvesting mote mycotoxin production in growing crops. In fact,
methods, pretreatments, sun drying, and solar drying on the changes in farming practices in the past few decades may
mold and mycotoxin contamination of Ž gs. These authors result in increasing stress on plants and therefore enhance
concluded that harvesting the fruits by hand and drying fungal invasion and mycotoxin contamination. For exam-
them as soon as possible with a solar drier minimizes en- ple, the push for larger crop yields has resulted in the plant-
vironmental contamination, results in homogenous drying, ing of crops more densely, with a resultant increase in com-
and is helpful in reducing a atoxin contamination in dried petition for water and the risk of water stress. Reduced
Ž gs as well as in improving other quality characteristics in genetic diversity within cultivars and large continuous acre-
comparison with those of samples treated otherwise. ages of the same cultivar may also result in plants being
more susceptible to stress from insects and disease pests
Moisture content and aw. A common feature of dried
(61). In conclusion, control management should begin in
fruits is that a low aw value is the basis for their preser-
the orchard and continue until the Ž nal product reaches the
vation. Minimum water requirements for fungal growth dif-
consumer.
fer depending on the temperature and on the substrate. The
minimum aw value for growth is lowest at the optimum Preharvest management. From a practical point of
temperature and highest near the minimum and maximum view, the best approach to eliminating mycotoxins from
growth temperatures (27). In general, the optimum aw value foods is to prevent mold growth at all levels of production,
for fungal growth is different from the aw value at which harvesting, transport, and storage. However, such an ap-
the maximum level of mycotoxin formation is observed. proach is not always as simple and straightforward as it
Table 6 shows the minimum aw values for the growth and may seem (26). Swanson (116) reported that preventive
mycotoxin formation of some potentially toxic molds. management on the farm includes the use of methods of
Several studies concerning the in uence of aw on my- cultivating to improve plant vigor, the judicious use of in-
cotoxin formation and fungal growth were conducted by secticides and fungicides, irrigation, and cultivar selection.
Northolt and coworkers (73–78). The minimum aw value These methods ensure that plants will be vigorous and less
for mycotoxin production by Penicillium species is higher vulnerable to stress, and they also help to limit the spread
than the minimum value for the production of a atoxin by of mold. With regard to the preventive measures to be taken
Aspergillus species. The production of penicillic acid was during the cultivation of fruits, Splittstoesser (106) reported
also restricted to high aw values (0.97 to 0.99), whereas that pruning, certain cultural and sanitary practices, and the
1524 DRUSCH AND RAGAB J. Food Prot., Vol. 66, No. 8

application of fungicides are the principal means for min- as, are dried after preservation with SO2 , which is essential
imizing infection and spoilage prior to harvest. Plant path- for the prevention of browning resulting from the Maillard
ogens may infect a variety of tissues in addition to the reaction. The high levels of SO2 also completely eliminate
fruits, and thus the removal of diseased branches and other the micro ora, even during prolonged storage.
plant parts helps to reduce the incidence of spoilage. Cul- Drying must start immediately after the harvesting of
tural practices that lower humidity in the growing area, such the crop and must be as rapid as possible. A safe moisture
as weed control and the proper spacing of plants, often have level must be reached before the crop is placed in storage.
a beneŽ cial effect because the growth of fungi is favored Buchanan et al. (25) studied the effect of the length of the
by moist conditions. Sanitation in the orchard and in the period between the infection and the drying of Ž g fruits.
vineyard is important for the control of spoilage organisms, These authors found that fruits allowed to dry on the tree
which may grow in cankers, dead branches, and fallen accumulated the highest levels of a atoxin (109 mg/g). A
fruits. delay of 72 h between inoculation and drying resulted in
Özay et al. (79) reported that the destruction of insects an a atoxin level of 74 mg/g, and a 24-h delay resulted in

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following the fertilization of fruits may be a promising an accumulation of 9.2 mg/g.
means for the reduction of plant pathogens. In addition, Dried fruits to be stored must be of high quality (free
orchards must be cleaned through the removal of decayed of molds, insects, and off-odors and dried to a safe moisture
material and other foreign materials. Although it does not level) whenever possible. During storage, insects can be
provide a general solution to the problem, irrigation may controlled with the use of fumigation, radiation, and good
also be a possible way to reduce A.  avus contamination, sanitary practices, while mold growth is best controlled
since A.  avus is known to be resistant to drought stress, with safe-moisture-level storage (50). It is important to
which affects other molds negatively (30, 85). maintain a constant temperature and relative humidity,
since moisture migration and condensation resulting from
Harvesting management. Harvesting of fruits in dry
thermal gradients within the stored bulk can cause an ac-
weather, careful handling, and minimization of mechanical
cumulation of moisture in certain areas in which mold
damage are important measures that can be taken to ensure
growth can occur. Low-temperature storage should be pre-
mycotoxin-free products (11). Splittstoesser (106) summa-
ferred, since mycotoxin contamination is directly correlated
rized some important control practices for the harvesting,
with temperature, except for some species of Fusarium that
grading, and packing stages as follows. (i) Harvest fruit
can produce mycotoxins at low temperatures; storage under
when it is at optimum maturity. (ii) Handle fruit gently to
nitrogen inhibits the growth of these Fusarium species (50).
prevent bruises and punctures that would permit the entry
Dried fruits must also be stored in structures or containers
of saprophytic fungi. (iii) Maintain good sanitation to min-
that are moisture proof and amenable to fumigation treat-
imize the buildup of mold on fruit contact surfaces. Me-
ment (11).
chanical harvesters, lug boxes, and packinghouse equip-
In conclusion, the mycotoxins that are most relevant to
ment should be cleaned and sanitized regularly. Treatment
fruits and fruit products are a atoxins, ochratoxin A, and
with live steam, treatment with formaldehyde, and fumi-
patulin. The extent of fungal growth and subsequent pos-
gation with chlorine gas are some of the measures taken to
sible mycotoxin contamination depends on endogenous fac-
destroy fungal spores. (iv) Remove moldy fruit, as well as
tors such as type of fruit, pH, and ripening state, as well as
fruit showing skin breaks and bruises, during the sorting
exogenous factors such as ambient temperature, relative hu-
and grading operations.
midity, and competing fungi. As discussed above, fungal
Processing management. Özay and Alperden (80) re- growth does not necessarily re ect the presence of myco-
ported that the use of UV lamps for sorting contaminated toxins. Conditions for mycotoxin production are more spe-
fruits out from sound ones seems like quite an efŽ cient ciŽ c, and even a prediction based on inoculation experi-
method for reducing the percentage of Ž gs contaminated ments is difŽ cult, since conditions associated with such ex-
with a atoxins. In a similar study, Steiner et al. (111) dem- periments re ect environmental conditions poorly.
onstrated that the sorting of fruits under UV light is simple The contamination of fruits with mycotoxins is likely
and fast and may easily be used to efŽ ciently ‘‘clean’’ large to result in contaminated fruit products. The careful selec-
batches of dried Ž gs on an industrial scale before retail tion and proper storage of fruits are the most important
distribution. The results obtained by Steiner et al. (111) factors in quality control. As shown for the preharvest man-
indicated that the elimination of all  uorescent Ž gs did not agement of dried Ž gs, harvesting and drying conditions and
result in the removal of all a atoxin-containing fruits. In measures taken during processing, such as the sorting of
fact, the  uorescence sorting method for whole fruits ex- fruits, in uence the degree of contamination within a batch.
cludes only fruits exhibiting  uorescence on the outer sur- The types mycotoxin contamination most frequently de-
face, not the internally contaminated fruits. scribed for dried fruits are a atoxin contamination of Ž gs
Özay et al. (79) found that the treatment of Ž g fruits and dates and ochratoxin A contamination of grapes.
with dipping solutions such as sodium metabisulŽ te, potas- As shown for patulin in apple juice, the removal of
sium metabisulŽ te, potassium sorbate, and hot (1008C) wa- mycotoxins can be achieved to a certain degree through
ter followed by prompt dehydration with a solar drier mark- physical or chemical measures taken during processing. For
edly decreased mold counts and a atoxin contamination. patulin, a further decrease during the storage of apple juice
Some fruits, including apricots, peaches, pears, and banan- has been observed. The structures of the resulting chemical
J. Food Prot., Vol. 66, No. 8 MYCOTOXINS IN FRUIT PRODUCTS 1525

compounds have not been elucidated. In view of the toxi- 21. Beretta, B., A. Gaiaschi, C. L. Galli, and P. Restani. 2000. Patulin
in apple-based foods: occurrence and safety evaluation. Food Addit.
cological potential of mycotoxins, future research may fo-
Contam. 5:399–406.
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ACKNOWLEDGMENT during apple juice clariŽ cation. J. Food Prot. 8:1216–1219.
23. Boyacioglu, D., and M. Gonul. 1990. Survey of a atoxin contam-
The preparation of this review was Ž nancially supported by the state ination of dried Ž gs grown in Turkey in 1986. Food Addit. Contam.
government of Schleswig-Holstein, Germany. 7:2, 235–237.
24. Brackett, R. E., and E. H. Marth. 1979. Ascorbic acid and ascorbate
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