1 Conditions Leading to Mycotoxin Contamination of Foods and Feeds CLIFFORD W. HESSELTINE
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Northern Regional Research Laboratory, Agricultural Research Service, U.S. Department of Agriculture, Peoria, Ill. 61604 Toxigenic mold invasion is affected during plant growth, at harvest, and after harvest. Invasion by fungi is affected by the amount of spore inoculum in the field, stresses on the plant, invertebrate infections, damage by other fungi, plant resistance, mechanical damage, mineral nutrition of the plant, and temperature. During harvest, grain is exposed to mechanical damage and mold inoculum. After harvest, mold growth depends on moisture level of the grain, temperature and humidity, rapidity of drying, aeration, the microbiological ecosystem, insects, mixing of grain, chaff and dirt, chemical treatment, internal infection, accidental rewetting of the grain by condensation or leakage, and the development of hot spots.
The key to preventing toxigenic fungi from developing in foods and feeds is to understand how they enter and develop in plant material. The alternative to preventing them from developing is to destroy or to remove the mycotoxin from the food or feed. However this approach is fraught with a number of problems: (a) any chemical or physical treat ment that removes mycotoxins adds to the cost of a product already damaged from mold growth; besides the initial processing cost, additional material may be lost from separating the mycotoxin-infected parts me chanically or chemically (solvent extraction). For example, scabby wheat is cleaned by removing the chaffy kernels, (b) Most processes that remove mycotoxins are not 100% efficient, (c) When chemical processes are used, extensive testing is required to establish that a second biologi cally active compound with a different mode of action has not been formed, (d) Processes that remove mycotoxins may reduce the food value of the final product. 1
In Mycotoxins and Other Fungal Related Food Problems; Rodricks, J.; Advances in Chemistry; American Chemical Society: Washington, DC, 1976.
2
MYCOTOXINS
I p r e f e r t h e first, a n d p e r h a p s less p o p u l a r , a p p r o a c h of p r e v e n t i n g m o l d f r o m d e v e l o p i n g i n crops.
H o w e v e r , this a p p r o a c h r e q u i r e s a t h o r
o u g h u n d e r s t a n d i n g of the c o n d i t i o n s u n d e r w h i c h e a c h of the m y c o t o x i n m o l d s grows—i.e., i n f o r m a t i o n f r o m one species of f u n g i c a n n o t b e t r a n s f e r r e d to a n o t h e r species. Pénicillium
duponti
has a n o p t i m u m g r o w t h at
45 ° C a n d does n o t g r o w at r o o m t e m p e r a t u r e , t h e o p t i m u m t e m p e r a t u r e for P . citrinum.
growth
O u r basic information about fungal growth
is s u r p r i s i n g l y m e a g e r a n d i n c o m p l e t e .
F o r example, early i n our w o r k
o n aflatoxin i n cereals, w e s e a r c h e d the l i t e r a t u r e f o r the k i n d of sugars t h a t Aspergillus
flavus
u t i l i z e d : w e f o u n d o n l y a short a n d i n c o m p l e t e
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statement o n t h e subject
(I).
I n this b r i e f r e v i e w of c o n d i t i o n s l e a d i n g t o m y c o t o x i n f o r m a t i o n i n foods a n d feeds, I u s u a l l y use o n l y one reference conserve
space; h o w e v e r ,
for each factor
I e n u m e r a t e a l l factors affecting
to
mycotoxin
f o r m a t i o n w i t h o u t d e s c r i b i n g the o p t i m u m c o n d i t i o n s f o r m a x i m u m p r o d u c t i o n of m y c o t o x i n s b y a n y p a r t i c u l a r m o l d species; I f o l l o w the o u t l i n e of J a r v i s ( 2 )
w h o d i v i d e d the e n v i r o n m e n t a l c o n d i t i o n s i n t o c h e m i c a l ,
physical, and biological. T a b l e I.
F u n g i W h i c h Produce Mycotoxins Classified by H a b i t a t
F u n g i G r o w i n g i n the L i v i n g P l a n t Claviceps purpurea Aspergillus flams Sclerotinia sclerotiorum Rhizoctonia leguminicola Fusarium graminearum Helminthosporium (Gibberella zeae) biseptatum Fungi Growing in Decaying Plant Material Fusarium graminearum Pithomyces chartarum Stachybotrys atra Chaetomium globosum Periconia minutissima Dendrodochium toxicum Fusarium sporotrichoides Myrothecium verrucaria Gladosporium sp. Trichothecium roseum Alternaria longipes Trichoderma viride F u n g i Growing on Stored P l a n t M a t e r i a l Pénicillium islandicum Aspergillus flavus P. citrinum A. parasiticus P. rubrum A. versicolor P. citreoviride A. ochraceus P. cyclopium A. clavatus P. viridicatum A. fumigatus P. urticae A. rubrum P. verruculosum A. chevalieri P. puberulum P. expansum P. rugulosum P. palitans P. roqueforti
Chaetomium globosum Fusarium graminearum F. tricinctum F. nivale F. moniliforme
In Mycotoxins and Other Fungal Related Food Problems; Rodricks, J.; Advances in Chemistry; American Chemical Society: Washington, DC, 1976.
1.
HESSELTiNE
Conditions
Leading
to
3
Contamination
A n o t h e r a p p r o a c h is to s t u d y t h e different c o n d i t i o n s w h i c h i n f l u e n c e m o l d g r o w t h i n t h e field a n d d u r i n g t h e h a r v e s t a n d storage. a m p l e , factors affecting m o l d i n v a s i o n of t h e d e v e l o p i n g
F o r ex
corn kernel
i n c l u d e the a m o u n t of spore i n o c u l a , stress factors o n the g r o w i n g p l a n t , insect a n d m i t e p o p u l a t i o n s , d a m a g e f r o m other f u n g i , v a r i e t a l s u s c e p t i b i l i t y o r resistance, m e c h a n i c a l d a m a g e f r o m f a r m i n g , s t o r m
damage,
b i r d d a m a g e , m i n e r a l n u t r i t i o n of t h e p l a n t , a n d t e m p e r a t u r e .
During
harvest, the g r a i n is e x p o s e d to m e c h a n i c a l i n j u r y a n d extensive s p o r e i n o c u l a t i o n . A f t e r harvest, m o l d g r o w t h a n d m y c o t o x i n p r o d u c t i o n c a n b e affected b y the m o i s t u r e l e v e l , t e m p e r a t u r e , a e r a t i o n , m i c r o b i o l o g i c a l Downloaded by AKDENIZ UNIV on December 20, 2014 | http://pubs.acs.org Publication Date: June 1, 1976 | doi: 10.1021/ba-1976-0149.ch001
ecosystem, storage insects, b l e n d i n g of c o r n , a m o u n t of chaff a n d d i r t , c h e m i c a l treatment, a m o u n t of i n t e r n a l i n f e c t i o n , r e w e t t i n g f r o m c o n d e n s a t i o n a n d l e a k a g e , a m o u n t of
damage,
chemical composition
of
the
substrate, a n d h e a t i n g . M y c o t o x i n p r o d u c t i o n is also a v a r i a b l e f a c t o r . Numerous fungi produce mycotoxins
i n the l i v i n g p l a n t , o n
plant material, a n d i n stored m a t e r i a l ( T a b l e I ) .
decaying
T a b l e I I contains t h e
p h y s i c a l , c h e m i c a l , a n d b i o l o g i c a l factors that influence m o l d g r o w t h a n d mycotoxin formation. Table II.
Factors Affecting M y c o t o x i n Formation
Physical Moisture r a p i d i t y of d r y i n g rewetting relative h u m i d i t y Temperature M e c h a n i c a l damage B l e n d i n g of g r a i n H o t spots Time Chemical C0 0 N a t u r e of substrate Mineral nutrition Chemical treatment 2
2
Biological P l a n t stress Invertebrate vectors F u n g u s infection P l a n t v a r i e t a l differences F u n g a l s t r a i n differences Spore l o a d M i c r o b i o l o g i c a l ecosystem
In Field
At Harvest
+ —
+ + + + + + + — +
+ + + + + + + + +
— — — —
+ + + + +
—
+ + + — —
+ — —
+ + — + + + + + + +
In
—
— — — — —
+ —
In Mycotoxins and Other Fungal Related Food Problems; Rodricks, J.; Advances in Chemistry; American Chemical Society: Washington, DC, 1976.
Storage
+ + + + + + +
4
MYCOTOXINS
Physical
Factors
M o i s t u r e . I f o t h e r factors are e q u a l , t h e s a p r o p h y t i c f u n g i t h a t g r o w i n the field r e q u i r e a h i g h e r m o i s t u r e l e v e l t h a n those f o u n d i n storage. Jarvis (2)
states t h a t d e c a y f u n g i r e q u i r e a h i g h e r m o i s t u r e c o n t e n t i n
t h e substrate ( 2 2 - 2 5 %
w e t w e i g h t ) t h a n storage f u n g i , w h i c h c a n g r o w
o n s t o r e d substrates ( 1 3 - 1 8 % ) . T w o aspects of t h e effect of m o i s t u r e o n f u n g i m u s t b e c o n s i d e r e d : the m o i s t u r e r e q u i r e d f o r spore g e r m i n a t i o n , a n d moisture r e q u i r e d for growth.
T h e r e is s o m e suggestion t h a t a n
o p t i m a l m o i s t u r e l e v e l exists f o r aflatoxin f o r m a t i o n i n s o l i d substrates.
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S u s s m a n ( 3 ) cites a n u m b e r of references to f u n g i , s u c h as Fusarium
and
w h o s e spores w i l l n o t g e r m i n a t e w i t h o u t a n exogenous
Myrothecium,
source o f e n e r g y e v e n t h o u g h m o i s t u r e levels are a d e q u a t e a n d spores c o n t a i n a n e n e r g y source. O n t h e other h a n d , spores of some f u n g i , s u c h as the r u s t f u n g i a n d Helminthosporium, A y e r s t (4)
germinate i n distilled water.
s t u d i e d the effect of m o i s t u r e o n the g r o w t h of a n u m b e r of
f u n g i . H i s d a t a o n t h e m y c o t o x i n - p r o d u c i n g f u n g i are s h o w n i n T a b l e I I I . Table III. Approximate Temperature and Moisture Limits and O p t i m a f o r G r o w t h of S e v e r a l M y c o t o x i n - P r o d u c i n g F u n g i " Limits
Optima
aw
°C
aw*
Species
10-42 0.71 Aspergillus chevalieri 0.93 33 0.78 12-43 0.98 Aspergillus flavus 33 0.82 12-53 0.97 40 Aspergillus fumigatus 0.82
