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DOI: 10.1177/1040638713504572
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Article
Introduction
Mycotoxicoses are important diseases of ruminants and
horses. In South America, where pastoral farming systems
predominate, there have been a number of studies published
regarding mycotoxicoses of ruminants and horses; however,
most of this information has been published in Spanish or
Portuguese in journals of limited circulation or in meeting
proceedings. The current review reports the epidemiology,
clinical signs, and pathology of the main mycotoxicoses
affecting livestock, mainly in South America, with an empha-
sis on the information necessary for the diagnosis of poison-
ing (Tables 1, 2). Comparisons are also made with the
occurrence of the same mycotoxicoses on other continents. A
description of the details of the laboratory techniques for
toxin detection is beyond the scope of this review.
Poisoning by indole-diterpenoid
mycotoxins
The 3 main grasses that cause tremorgenic syndrome due to
the presence of indole-diterpenoid alkaloids are Paspalum
spp., Cynodon dactylon, and Lolium perenne. Paspalum
staggers occurs when Claviceps paspali invades the unfertil-
ized ovaries of Paspalum spp. during flowering time, replac-
ing them with a mass of fungal tissue named sclerotia
(Fig. 1A).66 The main indole-diterpenoid tremorgens in
C. paspali are paspalinine and paspalitrems A–C.17 This
mycotoxicosis occurs in southern Brazil,66 Uruguay,56 Argen-
tina,36 the United States,17 Australia,39 New Zealand,80
Europe,5,44 and South Africa.9,81 Several species of Paspalum
can be infected by C. paspali, including Paspalum dilatatum
Poiret, Paspalum notatum Flügge, and Paspalum distichum
L. (syn. Paspalum paspalodes [Michx.] Scribne), Paspalum
vaginatum Sw, Paspalum scrobiculatum L., and Paspalum
urvillei Steud. In South America and other countries of the
southern hemisphere, poisoning occurs from the end of Feb-
ruary until early June (i.e., between the end of summer and
the start of autumn), when Paspalum spp. is seeding. The
disease occurs mainly in rice stubbles 1–2 years after harvest,
XXX10.1177/1040638713504572Mycotoxicoses of ruminants and horsesRiet-Correa et al.
research-article2013
From the Hospital Veterinário, Centro de Saúde e Tecnologia Rural,
Universidade Federal de Campina Grande, Patos, Paraíba, Brazil (Riet-
Correa, Medeiros); Dirección de Laboratorios Veterinarios “Miguel
C. Rubino”, Laboratório Regional Noroeste, Ministério de Ganadería,
Agricultura y Pesca, Paysandú, Uruguay (Rivero); Instituto Nacional de
Tecnología Agropecuaria, Estación Experimental Agropecuaria Balcarce,
Balcarce, Argentina (Odriozola); Faculdade de Veterinária, Universidad de
la República, Estação Mario Cassinoni, Paysandú, Uruguay (Adrien); and
Laboratório Regional de Diagnóstico, Faculdade de Veterinária, UFPel,
Pelotas, Rio Grande do Sul, Brazil (Schild).
1Corresponding Author: Franklin Riet-Correa, Veterinary Hospital,
Centro de Saúde e Tecnologia Rural, Federal University of Campina
Grande, Campus de Patos, Patos, Paraíba 58700-000, Brazil. franklin.riet@
pq.cnpq.br
Mycotoxicoses of ruminants and horses
Franklin Riet-Correa,1 Rodolfo Rivero, Ernesto Odriozola,
Maria de Lourdes Adrien, Rosane M. T. Medeiros, Ana Lucia Schild[AQ: 1]
Abstract. In the current study, mycotoxicoses of ruminants and horses are reviewed, with an emphasis on the occurrence of
these diseases in South America. The main mycotoxicoses observed in grazing cattle include intoxications by indole-diterpenoid
mycotoxins (Paspalum spp. contaminated by Claviceps paspali, Lolium perenne infected by Neotyphodium lolii, Cynodon
dactylon infected by Claviceps cynodontis, and Poa huecu), gangrenous ergotism and dysthermic syndrome (hyperthermia)
caused by Festuca arundinacea (syn. Festuca elatior) infected by Neotyphodium coenophialum (syn. Acremonium
coenophialum), and photosensitization in pastures contaminated by toxigenic Pithomyces chartarum. Other mycotoxicoses
in grazing cattle include slaframine toxicity in clover pastures infected by Rhizoctonia leguminicola and diplodiosis in cattle
grazing in corn stubbles. The mycotoxicoses caused by contaminated concentrated food or byproducts in cattle include
poisoning by toxins of Aspergillus clavatus, which contaminate barley or sugar beetroot by-products, gangrenous ergotism or
dysthermic syndrome caused by wheat bran or wheat screenings contaminated with Claviceps purpurea, and acute respiratory
distress caused by damaged sweet potatoes (Ipomoea batatas). The main mycotoxicosis of horses is leukoencephalomalacia
caused by the fumonisins B1 and B2 produced by Fusarium spp. Poisoning by C. purpurea and F. elatior infected by N.
coenophialum has also been reported as a cause of agalactia and neonatal mortality in mares. Slaframine toxicosis caused by
the ingestion of alfalfa hay contaminated by R. leguminicola has also been reported in horses.
Key words: Aspergillus clavatus; ergotism; indole-diterpenoid mycotoxins; Ipomoea batatas; leukoencephalomalacia;
Pithomyces chartarum; slaframine.
Riet-Correa et al.
2
in cultivated pastures 3–4 years after establishment when the
Paspalum spp. substitute the species planted, and in natural
pastures with highly fertile soil, such as marshy or irrigated
areas.36,56,66 Cattle of various ages and categories, as well as
buffalo5 and horses,15 can be affected.
Poisoning by consumption of C. dactylon L. has been
reported in cattle in Uruguay,57,70 Argentina,46 the United
States,16 and South Africa81 and in horses in California.16 In
South Africa, it was determined that the toxicity of this spe-
cies was due to infection with Claviceps cynodontis, which
contains a mixture of indole-diterpenes, of which paspalit-
rems A and B, as well as paspaline and paspalinine, repre-
sented major constituents.81 In the South American countries,
the disease occurs mainly in the winter months (July and
August) when the seeding plant is dry due to severe frosts.
Cynodon dactylon is a weed of pastures, crops, and degraded
areas. Poisoning occurs mainly in pastures severely invaded
by C. dactylon, where this plant becomes the only grass
available.
Ryegrass staggers is caused by the endophytic fungi Neo-
typhodium lolii (syn. (Acremonium lolii) in perennial rye-
grass (Lolium perenne).75,80 The main indole-diterpenoid
tremorgens found in L. perenne are paxilline and lolitrems,
primarily lolitrem B,23,30,71,80 which are believed to act on
γ-aminobutyric acid receptors disrupting neuromuscular
control.43 Neotyphodium lolii also produce ergopeptide alka-
loids, which have been associated with reduced milk produc-
tion due to prolactin depression in cattle and sheep,
hyperthermia and heat stress in sheep during the summer,
and other signs such as reduction of weight gains and fecal
contamination of wool (dags) in lambs (Duringer JM, DeLo-
rme MJM, Lehner A, et al.: 2007, A review of the ergot alka-
loids found in endophyte-infected tall fescue and perennial
ryegrass and their metabolism after ingestion by livestock.
In: Proceedings of the 6th International Symposium on Fun-
gal Endophytes of Grasses: no. 13. Fungal endophytes of
grasses, ed. Popay AJ, Thom ER, pp. 377–382. Dunedon
New Zealand Grassland Association, New Zealand).23,30,80
Neotyphodium lolii also produces peramine, which confers
resistance against insects including the Argentine stem wee-
vil (Listronotus bonariensis).23,71,80 Ryegrass staggers occurs
frequently in New Zealand and Australia but has been
reported in the United States, Europe, South Africa, and
Argentina in sheep, cattle, deer, and horses.47,80 The effects
of ryegrass staggers are most serious during the summer and
autumn, when the shortage of forage forces livestock to
Table 1. Main features for the diagnosis of mycotoxicosis in grazing livestock in South America.*
Disease/agent
Species
affected Substrate/toxin Epidemiology Clinical signs Pathology Diagnosis
Ryegrass staggers;
Neotyphodium lolii
Bovine, ovine,
equine,
camelid
Lolium
perenne;
indole-
diterpenes
During summer
and autumn
in overgrazed
pastures
Tremors NSL Clinical signs; presence
of plant; toxin and
endophyte identification
Paspalum staggers;
Claviceps paspali
Bovine,
equine,
buffalo
Paspalum
spp.; indole-
diterpenes
During autumn
at seeding
Tremors NSL Clinical signs; presence
of plant with infected
seeds
Bermuda grass
staggers; Claviceps
cynodontis
Bovine, equine Cynodon
dactylon;
indole-
diterpenes
During winter
after frosts
Tremors NSL Clinical signs; presence
of plant
Ergotism;
Neotyphodium
coenophialum
Bovine, ovine,
equine
Pure pastures
of Festuca
elatior; ergot
alkaloids
During winter Gangrenous
ergotism
Necrosis of
distal limbs
Clinical signs; presence
of plant; toxin and
endophyte identification
During summer Dysthermic
ergotism
NSL
Pithomycotoxicosis;
Pithomyces
chartarum
Bovine, ovine,
deer
Clover/
gramineae
pastures
with dead
plant matter;
sporidesmin
Mainly in
autumn with
rains and
temperatures of
approximately
24°C
Dermatitis
and hepatic
insufficiency
Liver
degeneration
and fibrosis
Clinical signs; pathology;
spore counting;
demonstration of spore
toxigenicity
Slobbers;
Rhizoctonia
leguminicola
Bovine,
equine,
caprine
Pastures or hay
of red clover
and alfalfa
During autumn
with excessive
rainfalls
Salivation NSL Clinical signs; fungi
observation; toxin
detection
Diplodiosis;
Stenocarpella
maydis
Bovine, ovine Corn stables;
diplonine
By consumption
of cob, leaves,
and stem of
maize
Nervous signs NSL Clinical signs; presence
of fungi
* NSL = nonsignificant lesions.
Mycotoxicoses of ruminants and horses 3
ingest the basal sheath region of the plant, which contains the
highest lolitrem concentrations. The poisoning can also be
caused by ryegrass hay and ryegrass seed screenings. Neoty-
phodium lolii is transmitted only through the seeds, so the
infection is not spread between plants. However, because the
infected plants are more resistant to drought and insect
attacks, they produce a greater number of infected seeds, and
the infection occurs more frequently in the new plants,
increasing the toxicity of the pasture over time.23,39
Another endophyte-related disease associated with tremo-
ring in South America is poisoning by Poa huecu, which has
been reported in Argentina. Paxilline has been identified in
this type of poisoning, suggesting that the tremors are caused
by indole-triterpenoid alkaloids (Towers RN: 1994, Corne-
zuelo e endofitos como causa de síndromes nerviosos y
asoleamento en especies pecuarias [Ergot and endophytes
causing nervous diseases and hyperthermia in livestock]. In:
Buiatrics Uruguayan XXII Conference. Centro Médico vet-
erinário Paysandú, Uruguay, pp. C1–C10. In Spanish).
Poisoning by indole-diterpenoids contained in Paspalum
spp., C. dactylon, and ryegrass cause similar clinical signs,
which are characterized initially by fine tremors and discrete
head nodding, and can be exacerbated by excitement or
movement. Later, the animals display cerebellar ataxia with
severe tremors, uncoordinated gait with rigid legs, hyperme-
tria, swaying when standing, and a wide-based stance. When
affected animals are driven or startled, they can fall to either
side, forward or backward, sometimes into unusual posi-
tions, and occasionally paddle violently during vigorous
attempts to rise (Fig. 1B). After a period of rest, the animals
usually rise unassisted. In the more affected animals, tremors
became generalized. Generally, the appetite is maintained,
but weight loss occurs. Hypersensitivity to noise or move-
ment is also observed. Severely affected animals may
become recumbent, with generalized tremors, opisthotonus,
nystagmus, and salivation. When the animals are removed
from pastures, full regression of clinical signs occurs in 7–15
days. Some animals have died as a consequence of accidents
or while remaining recumbent.36,46,56,57,66,80
No gross lesions are observed following intoxication, but
in the case of Paspalum staggers, many Paspalum seeds are
observed in the abomasum contents. Most cases have no his-
tological lesions, but some cases with a more prolonged
clinical manifestation period have cerebellar lesions, with
degeneration and loss of Purkinje cells and the presence of
axonal spheroids in the granular layer.38,66
Table 2. Main features for the diagnosis of mycotoxicosis in livestock ingesting grains or grain by-products in South America.*
Disease/agent
Species
affected Substrate/toxin Epidemiology Clinical signs Pathology Diagnosis
Ergotism; Claviceps
purpurea
Bovine,
equine
Ergot in
grains or
byproducts;
ergot
alkaloids
Grain
byproducts
contaminated
by ergotized
Lolium
multiflorum
Mainly
dysthermic
ergotism; less
frequently,
gangrenous
ergotism
NSL Clinical signs;
presence of
ergot and ergot
alkaloids
Aspergillus clavatus Bovine, ovine Barley and
sugar beet
residues;
patulin and
other toxins
Improper
storage of
barley, barley
residues, or
beet residues
Nervous
signs and
recumbence
Neuronal
degeneration
Clinical signs;
histopathology;
multitoxin and
patulin analysis;
isolation of A.
clavatus
Aflatoxicosis; Aspergillus
flavus, and others
Bovine,
equine,
caprine
Grains or
byproducts;
aflatoxins
B1, B2, G2,
and G2
Feeding
with grains
and grain
byproducts;
also in
nonharvested
maize
Unspecific signs
of hepatic
insufficiency;
low milk
production and
weight gains
Liver fibrosis,
megalocytosis,
and bile duct
proliferation
Lesions and
aflatoxin
quantification in
the food
Poisoning by moldy sweet
potatoes; Fusarium spp.
Bovine Damaged
sweet
potatoes;
3-substituted
furans
Ingestion of
damaged
sweet potatoes
Acute severe
respiratory
signs
Pulmonary
emphysema
and edema
Ingestion of sweet
potatoes; clinical
signs
Leukoencephalomalacia;
Fusarium verticillioides
Equine Corn and corn
byproducts;
fumonisins
B1, B2
Corn as main
food source
Severe acute
nervous signs
Malacia of the
white matter of
the brain
Corn ingestion;
clinical signs;
lesions
* NSL = nonsignificant lesions.
Riet-Correa et al.
4
This mycotoxicosis is diagnosed by observation of the
characteristic clinical signs and the presence of Paspalum
spp. infected by C. paspali, C. dactylon, or L. perenne. The
main diseases to be considered during differential diagnosis
is poisoning by Ipomoea asarifolia, which causes an identi-
cal tremorgenic syndrome in ruminants in northeastern Bra-
zil, and poisoning by Phalaris spp., which also causes
tremors in ruminants in South America62 and other countries.
In Phalaris spp., the presence of a characteristic pigmenta-
tion of the brain helps in the differential diagnosis of poison-
ing. Similar signs are observed following the ingestion of
crops or their byproducts containing indole-diterpenoid tox-
ins produced by fungi of the genera Aspergillus and Penicil-
lium.16 Other diseases that should be considered in the
differential diagnosis are hypomagnesaemia, poisoning by
swainsonine-containing plants, and cerebellar degeneration
caused by Solanum spp.62
Currently, there is no effective treatment for poisoning.
The whole herd, or at least animals showing clinical signs,
should be gently removed from the infected pastures. In the
case of Paspalum staggers, the prevention of intoxication
should focus on the suppression of inflorescence. Slashing or
mowing may be used to remove seed heads. Paspalum spp.
are tolerant of heavy grazing, so high grazing pressure should
be maintained during the summer to prevent heavy seeding.
High grazing pressure also helps decrease soil contamination
by ergot and prevents heavy infection for the next year (Riet-
Correa F, Rivero R, Dutra F, et al.: 2007, Micotoxicosis en
animales domésticos en pastoreo [Mycotoxicosis in grazing
domestic animals] In: Jornadas Uruguayas de Buiatría, Pay-
sandú. Buiatrics Uruguayan XXXV Conference, Paysandú,
Uruguay, vol. 35, pp. 116–131). The only way to prevent C.
dactylon poisoning is to avoid grazing livestock in severely
infected pastures during the winter. Nevertheless, the risk of
C. dactylon poisoning is very low, because despite the
numerous pastures invaded by this species in South America,
poisoning is rare. The prevention of ryegrass staggers is
based on the avoidance of heavy grazing during the dry sea-
son, thereby forcing livestock to graze the lower part of the
pastures. Pastures that are at least 30 cm high can be consid-
ered nontoxic. Pastures infected with L. perenne can be
replaced by noninfected ryegrass, but this measure is unsuc-
cessful because compared to infected ryegrass, noninfected
ryegrass is more susceptible to environmental conditions and
less resistant to nematodes and insects. As a consequence,
noninfected ryegrass dies and is substituted by endophyte-
infected plants, which originate from seeds remaining in the
soil. Another possible solution is to replace toxic ryegrass
with seeds infected by a strain of N. lolii, which do not pro-
duces penitrems.23 AgResearch Ltd. developed AR6 novel
endophyte, which produces peramine and ergovaline to con-
trol the Argentine stem weevil and African black beetle (Het-
eronychus arator), but does not produce lolitrem B; however,
lambs on AR6 pasture could be more vulnerable to heat
stress due to ergovaline than lambs grazing endophyte-free
pastures.1
Ergotism
Ergot alkaloids produced by Claviceps purpurea and Fes-
tuca arundinacea Scribe (syn. Festuca elatior L.; tall fescue)
infected with Neotyphodium coenophialum (syn. Acremo-
nium coenophialum) cause diseases in ruminants and horses,
including gangrenous ergotism (also known as fescue foot in
cases of F. elatior poisoning), dysthermic ergotism (also
known as summer toxicosis, hyperthermia, idiopathic bovine
hyperthermia, and dysthermic syndrome), and a reproductive
form (causing agalactia or hypogalactia).6,10,35,59,65,77,80 Fes-
cue poisoning has also been associated with necrosis of the
abdominal fat in cattle.78 Nervous ergotism caused by C.
purpurea, as it is known in human beings, has not been fully
documented in domestic animals, and the reported cases
were most probably caused by indole-triterpene alkaloids in
Claviceps paspali.
Claviceps purpurea is a fungus that infects the ovaries of
crops and grass seeds, forming an sclerotium (ergot), which is
larger than the seeds, with a black or dark brown color and a
hard consistency (Fig. 2A, 2B). In South America, the fungus
can affect several species of grasses including Holcus lana-
tus, Setaria spp., Polypogon chilensis (syn. Chaetotropis
Figure 1. A, Paspalum notatum infected by Claviceps paspali.
B, bovine with nervous signs due to Cynodon dactylon poisoning.
Mycotoxicoses of ruminants and horses 5
Figure 2. A, Claviceps purpurea sclerotia infecting Festuca
elatior seeds. B, C. purpurea sclerotia compared with ryegrass
(left) and oat (right) seeds.
chilensis), Poa pratensis, Festuca spp., and Phalaris spp., but
most outbreaks in the region have been associated with the
ingestion of grains or their byproducts contaminated with
Lolium multiflorum L. (annual ryegrass) infected with C. pur-
purea.59 Lolium multiflorum is a weed that affects winter cul-
tures, mainly wheat; hence, the main cause of ergotism in
cattle in Uruguay is the contamination of wheat bran and
wheat screenings contaminated with annual ryegrass seeds
infected by C. purpurea (Fig. 2B). Oats harvested from areas
severely contaminated by C. purpurea–infected ryegrass
have been responsible for outbreaks of agalactia and neonatal
mortality in horses.65 Ergotism has also been reported in ani-
mals grazing on ryegrass pastures severely contaminated by
C. purpurea.59
The toxicity of F. elatior is due to infection by the endo-
phyte fungus Neotyphodium coenophialum, which produces
ergot alkaloids.77 This mycotoxicosis is very important in the
southwestern United States but has also been reported in sev-
eral other countries,10,80 including Argentina (Villahoz MD,
Moras EV, Barboni AM, et al.: 1984, Reproductive problems
of pregnant mares grazing fescue pastures in Argentina. In:
Proceedings of 10th Congress on Animal Reproduction and
Artificial Insemination, vol. 2, pp. 100–102, June 10–14,
Urbana-Champaign, Illinois)35,50 and Uruguay.61 The endo-
phyte is transmitted only through the seed, but because non-
infected plants are less resistant to drought and environmental
stress, they die and are replaced by endophyte-infected plants
originating from seeds that remain in the soil.80
Ergot alkaloids are generally classified in 2 main groups:
ergoline alkaloids, which include lysergic acid, lysergol,
lysergic, acid amide, and ergonovine; and ergopeptine alka-
loids, which include ergotamine, ergocristine, ergosine,
ergocryptine, ergocornine, and ergovaline. Ergovaline is
probably the most active ergot alkaloid produced by N. coe-
nophialum, and the ergopeptine alkaloids ergotamine, ergo-
cristine, ergosine, ergocornine, and ergocryptine are the main
toxins in C. purpurea (Duringer JM, et al.: 2007, A review of
the ergot alkaloids).24,77
The vasoconstrictive effect of ergot alkaloids through
interactions with dopaminergic, adrenergic, and serotonergic
receptors cause constriction of the arterioles, resulting in gan-
grenous ergotism or hyperthermia.24 In temperate climates,
gangrenous ergotism occurs during the winter, and dysther-
mic ergotism occurs during the summer. In cold climates,
vasoconstriction causes ischemia, endothelial degeneration,
thrombosis, and ischemic necrosis.59 At temperatures higher
than 25°C, vasoconstriction of peripheral blood vessels
causes reduced blood flow to the skin, reducing heat loss
when ambient temperatures are high and leading to heat stress
and hyperthermia.16,59 In the reproductive form of ergotism in
horses, hypogalactia or agalactia occurs as a result of
decreased prolactin secretion and inhibition of mammary
gland development at the beginning of lactation or as a result
of lower milk production during lactation.6,24,77 A 2011 review
is available concerning the endocrine disruptive effects of
ergopeptine alkaloids on lactogenesis and steroidogenesis on
pregnant mares.24 Fibrosis and thickening of placenta are
most likely due to vasoconstriction of the placental vessels.6,65
Gangrenous ergotism and hyperthermia caused by C. pur-
purea31,59 and F. elation35,61 have been reported frequently in
cattle in Uruguay, Argentina, and southern Brazil. The repro-
ductive form of ergotism has been diagnosed in horses that
ingested C. purpurea in southern Brazil65 and Uruguay59 and
in horses that ingested F. elatior in Argentina (Villahoz MD,
et al.: 1984, Reproductive problems of pregnant mares graz-
ing fescue pastures). In Uruguay and southern Brazil, mor-
bidity due to hyperthermic ergotism varies from 25% to
70%, and, generally, spontaneous deaths do not occur.31,59
The morbidity of fescue foot can vary from 6% to 80%,
depending on the amount of tall fescue grass and the degree
of contamination. Fertilization with nitrogen and drought
stress can increase the toxicity of the grass.6 Lower weight
gains have also been observed in cattle without clinical
signs.80 Poisoning occurs at different times of the year, with
plants at different stages of growth. In cattle in Uruguay and
Argentina, the gangrenous form occurs in the winter, and
hyperthermic ergotism occurs in the summer. The disease
does not occur in paddocks with fescue contents below
50%.35 The occurrence of ergotism has become rare in Uru-
guay and Argentina, most likely due to the use of tall fescue
mixed with other grasses such as clovers and ryegrass and
also to the marketing of controlled seeds with endophyte
infection rates of less than 5%. In outbreaks of agalactia due
to C. purpurea ingestion, reported morbidity rates are
7–90%, with foal mortality rates of up to 50%.65
Riet-Correa et al.
6
In cattle, gangrenous ergotism is characterized by a dry
gangrene of the limb extremities. Initial clinical signs include
lameness with swelling and redness of the skin of the coro-
nary band and fetlock, and, in dairy cattle, reduced milk pro-
duction. Subsequently, the skin becomes gangrenous and
shows cracks, sometimes with purulent exudate under the
necrotic skin. Gangrenous lesions are separated from normal
skin by a clear line. The horn also separates from the under-
lying tissues, the skin sloughs off, and the rupture of tendons
and ligaments may result in loss of the hoof.59,61 The general
condition of animals is not greatly affected, although some
animals may show skin necrosis at the edge of the ears, the
tip of the tail, and the udder.59,61
Dysthermic ergotism in cattle is characterized by heat
stress with a high body temperature (40–42°C), rough hair,
dyspnea, decreased feed intake and weight gains, reduced
milk production, increased water intake, and polyuria. Diar-
rhea and nasal discharge are occasionally observed. When
environmental temperatures increase, affected cattle seek out
any shade available, stay in water ponds, and show severe
respiratory distress with an extended neck, open mouth,
drooling, and tongue exposition. During the hotter hours of
the day, the clinical signs are more evident than during the
night or on cold days. Some animals may show signs of
lameness and gangrenous ergotism in the limbs, ears, and tail
30–60 days after ingestion. Death can occur when infected
animals are exposed to ambient temperatures of more than
30°C. With the withdrawal of the contaminated food, the
clinical signs disappear slowly over a course of 2–3 weeks.
Abortions, agalactia, retained placenta, and reproductive
failures such as infertility and anestrus may occur during and
after the occurrence of hyperthermic ergotism.31,59,61
In cases of F. elatior poisoning in cattle, adipose tissue
necrosis in the abdominal cavity has also been described. This
change is detected by rectal palpation as hard masses that
range from 1 cm in diameter to large masses that are only
partially palpated on the dorsal surface. Such lesions, which
may or may not occur simultaneously with dysthermic ergot-
ism, may cause digestive disorders and calving problems.78
Gangrenous ergotism is a rare disease in sheep,34 but
digestive lesions can be observed in sheep experimentally
poisoned by C. purpurea.22 Poor weight gains and hyperther-
mia can be observed in sheep grazing tall fescue and in lambs
grazing perennial ryegrass contaminated by N. lolii, which
also produces ergot alkaloids.59,80 In horses, mainly in mares
during the last month of gestation, the main form of ergotism
is reproductive and is characterized by a lack of mammary
gland development and agalactia. In most cases, agalactia is
permanent after birth, but some mares can produce milk after
parturition if ergot alkaloids are removed from the food. Pre-
mature release of the chorioallantoid also occurs, and the
placenta is heavier, thickened, and fibrotic and must be man-
ually broken. Gestation may be prolonged, and some mares
have dystocia. Abortion, embryonic death, and anestrus have
also been reported.6,65 The foals born to affected mares are
weak, without mammary reflex, and neonatal mortality can
be higher than 50%.65 Newborn foals had decreased serum
triiodothyronine concentration, hypothyroidism, and signs of
dysmaturity, including marked decrease in muscle mass,
long fleshy hooves, and delayed eruption of incisor teeth.6,7
After the removal of food contaminated by ergot alkaloids,
the frequency of agalactia, other reproductive signs, and neo-
natal mortality rapidly decreases.65
Histologically, the lesions of gangrenous ergotism display
coagulation necrosis of the skin and subcutaneous tissue,
with proliferation of granulation tissue in the deeper layers.
The muscular layer of arterioles is hyperplasic, with narrow-
ing of the vessel lumen and of subcutaneous tissue.59 In the
reproductive form in horses, placental lesions are character-
ized by a thickening of the allantochorion and the degenera-
tion of the chorionic epithelium. In foals, jaundice and
enlarged, yellow livers with severe vacuolation of hepato-
cytes can be observed.65 No macroscopic lesions have been
reported in cases of hyperthermic ergotism in cattle. Histo-
logically, the only lesions observed in the cases described in
Brazil were pulmonary emphysema and hypertrophy of the
muscular layer of the bronchioles.31
The diagnosis of ergotism must be established by clinical
signs, pathological changes, and the presence of C. purpurea
sclerotia in the food or F. elatior contamination by N. coeno-
phialum, which can be confirmed by microscopic observa-
tion of leaf sections stained with aniline blue. The
determination of the number of infected plants is important
for confirmation of the diagnosis and to provide an indica-
tion of the toxicity of a pasture of tall fescue. Clinical signs
are likely to occur when at least 50% of the plants in a pas-
ture are infected. Infection of 15% of the plants can lead to a
reduction in daily weight gains. Milk production may be
affected in some animals when the ambient temperature is
high and 8% of the plants are infected.61 However, the per-
centage of infected plants is not the only factor that deter-
mines the toxicity of a pasture. Other factors, such as the
botanical constitution, the percentage of fescue, and the
nitrogen fertilization of the pasture, as well as the duration
and type of grazing animal, can influence the toxicity. The
diagnosis of C. purpurea presents difficulties when animals
are fed with products or ground-based grains, in which the
milled sclerotia cannot be identified. In such cases, labora-
tory tests are needed to detect the presence of C. purpurea or
ergot alkaloids. Ergot alkaloids can be identified in food by
thin-layer chromatography, enzyme-linked immunosorbent
assays, and high-performance liquid chromatography.10,33
Urinary ergot alkaloids can be determined in animals that are
still ingesting the contaminated food.10
After diagnosis of the disease, grazing animals should be
removed from fescue pastures infected by N. coenophialum
or ryegrass pastures contaminated by C. purpurea. Contami-
nated feed should also be removed from penned animals.
Treatment should be symptomatic; gangrenous lesions are
slowly reversible in milder cases but are not reversible in
Mycotoxicoses of ruminants and horses 7
Figure 3. Bovine with severe dermatitis due to pithomycotoxicosis.
Inset: spore of Pithomyces chartarum. Bar = 30 µm.
severe cases. For the prevention of gangrenous ergotism,
grains or byproducts should be inspected for the presence of
C. purpurea. As a weed in crops, L. multiflorum should be
controlled by the use of herbicides, which is difficult due to
increasing resistance to herbicides. Crop seeds should be free
of ryegrass seeds. In areas invaded by ryegrass, the preven-
tion of seeding will prevent soil contamination by ergot,
which can overwinter to infect ryegrass the following year.
Endophyte-free fescue seeds are available or can be
obtained by treating seeds with fungicides or by using seeds
after 12–15 months of storage. In Uruguay, fescue seeds
must have infection rates below 5%.61 Endophyte-free fescue
provides excellent livestock performance, but is less resistant
to drought and insect attacks.80 If endophyte-free fescue is
planted in an area previously occupied by infected fescue,
the culture will rapidly revert to an endophyte-infected pas-
ture as seeds in the soil germinate and the endophyte-free
plants die.80 A better approach is the use of fescue infected by
endophytes, called novel endophytes, which produce little or
no ergot alkaloids but still produce toxins against insects.3,80
The only way to use toxic pastures is to allow grazing only
for short periods, alternating grazing fescue pastures with
other species. However, one should consider the possibility
of lower weight gains and a drop in production.
Intoxication by Pithomyces chartarum
(pithomycotoxicosis)
Pithomyces chartarum is a saprophytic fungus distributed in
temperate, subtropical, and tropical regions. It is usually
found on dead vegetable matter at the base of the pasture.
The spores (Fig. 3) of pathogenic strains of the fungus pro-
duce sporidesmins A–H, but sporidesmin A is the most clini-
cally relevant. Sporidesmins B–H are of low biologic
significance. Sporidesmin causes cholestasis and pericholan-
gitis, resulting in hepatic photosensitization of sheep, cattle,
deer, and camelids. The poisoning, known as facial eczema,
is an important disease in New Zealand in perennial ryegrass
pastures, but has also been reported in the United States,
Canada, England, South Africa, The Netherlands, Uruguay,
and Argentina.75,80 In New Zealand, the disease is more com-
mon in sheep than in cattle. In contrast, pithomycotoxicosis
has only been reported in cattle in Uruguay and Argentina
because sheep are rarely grazed in cultivated pastures with
high productivity (Riet-Correa F, et al.: 2007, [Mycotoxico-
sis in grazing domestic animals]).45,54 In Brazil, many out-
breaks of hepatogenous photosensitization caused by
Brachiaria spp. were misdiagnosed as pithomycotoxicosis,
but it is now well known that the toxicity of Brachiaria spp.
is caused by steroidal lithogenic saponins,58 and almost none
of the P. chartarum strains from Brazil and Colombia pro-
duce sporidesmin.11,18 Analyses carried out in P. chartarum
isolated from pastures of Uruguay showed that 60% of the
strains were pathogenic (Towers N: 1994, Eczema facial
[Facial eczema]. In: Buiatrics Uruguayan XXII Conference,
Paysandú, Uruguay. Centro Médico veterinário Paysandú,
Uruguay, pp. G1–G9. In Spanish). In contrast, nearly all New
Zealand isolates produce sporidesmin.18
Pithomycotoxicosis has been detected since the 1970s in
Uruguay and Argentina,45,50,54 where it is the main cause of
hepatogenic photosensitization. This disease occurs in culti-
vated pastures of white, red, or subterranean clover mixed
with ryegrass (Lolium rigidum), Festuca arundinacea,
Phalaris spp., Avena sativa, or other gramineae. The follow-
ing 2 epidemiological conditions are necessary for pastures
to be toxic: environmental conditions must be favorable for
fungal growth, and pathogenic strains of P. chartarum, capa-
ble of producing sporidesmin, must be present. For the fun-
gus to multiply, conditions with suitable humidity and
temperature are required, as well as a suitable and abundant
substrate. The most favorable conditions for fungal growth
occur during cloudy days with rain, temperatures above
16°C (optimal temperature is 24°C), and relative humidity of
more than 80%. The repetition of these favorable growth
conditions significantly increases the number of spores. In
South America, outbreaks occur in the late summer and
autumn, when climatic conditions and pastures are suitable
for fungal growth.54 Intensive grazing practices facilitate the
ingestion of large numbers of spores present in the pasture
litter. Pastures with plenty of dead plant material, as in those
used for seed production, mixed pastures with wheat or oats,
pastures that cannot be baled due to adverse weather condi-
tions, and pastures that have been mowed can become toxic.
Hay produced from contaminated pastures or pastures that
receive rain may also be toxic, as can round bales that are
exposed to rain or high humidity levels.54
The toxicity of pastures depends on the number of toxic P.
chartarum spores in the dead plant material and the toxicity
of the individual P. chartarum strains. More than 40,000
spores of pathogenic strains per gram of dead vegetation can
cause photosensitivity, leading to a severe drop in milk pro-
duction, while 100,000 spores/g can lead to death.54 In Uru-
guay, the disease was very frequent from 1970 to 2000, but
the number of outbreaks has decreased, most likely due to
the use of high-quality soils, previously used for pastures, for
Riet-Correa et al.
8
grain production. Morbidity is variable, with rates of 5–10%,
while mortality ranges from 1% to 10%.54
In cattle, the first clinical signs may be transient diarrhea,
depression, anorexia, and severe reductions in milk yields
from milking cows. Subsequently, subcutaneous edema can
be observed, followed by dermatitis affecting exposed, non-
pigmented, uncovered areas of the skin (perineum, external
face of the udder, nose and muzzle, lips, ears, and periorbital
region; Fig. 3). Jaundice, salivation, and nasal and ocular dis-
charges are frequent. The tongue may be ulcerated on the
ventral surface, because of exposure to the sun when the ani-
mal licks its nostrils. Some affected animals seek shade, have
continuous movements of the head, and exhibit other signs
of pain. Sometimes the skin peels from a large area, mainly
on the face. More severe cases may be fatal during the acute
phase, without presenting photosensitization. Intravascular
hemolysis, anemia, hemoglobinuria, and abortions have also
been described.54 In sheep, the most characteristic sign is
dermatitis of the face; hence, the disease is called facial
eczema. The ears are edematous, and the animals display
photophobia and seek out any available shade. Jaundice,
subcutaneous edema, and other signs of liver failure are also
observed. Acutely affected sheep and cattle can die without
presenting photosensitization. In severe cases, edema, hem-
orrhages, and even necrosis may be observed in the urinary
bladder.54,75,80
The serum activities of gamma-glutamyl transferase and
aspartate aminotransferase and the serum concentrations of
bilirubin are increased in affected animals. Gamma-glutamyl
transferase is the best indicator of the disease, and high
serum concentrations may persist for periods of 3–6 months.
During outbreaks, the analysis of blood enzyme activities
may reveal that most animals without clinical signs are suf-
fering liver damage with production losses and increased
susceptibility to other diseases. Resistant animals show no
increase in serum gamma-glutamyl transferase activities.80
In acute cases, jaundice occurs, and the liver is yellowish
and enlarged. The gallbladder is also enlarged and shows
edema of the wall. In cases of longer evolution, the liver may
be yellowish or whitish due to periportal fibrous tissue pro-
liferation. These lesions are most marked in the left lobe,
which in chronic cases may be atrophic and fibrous.54,80 His-
tologic changes primarily affect the bile ducts, causing
degeneration and necrosis of the epithelium, followed by
proliferation of epithelial bile duct cells and periportal fibro-
sis. The periportal hepatocytes may show diffuse vacuoliza-
tion or necrosis. In chronic cases, there is severe periportal
fibrosis and atrophy of the parenchyma.54,80
Presumptive diagnosis is based on clinical signs and the
occurrence of the disease in pastures with dead plant mate-
rial, especially during the fall. The macroscopic and histo-
logical lesions are also suggestive of the diagnosis, but the
spores in the pasture must be counted for confirmation.
However, because not all strains of P. chartarum produce
sporidesmin, at least in regions where the disease has not
been previously diagnosed, it is also necessary to know if the
strains are sporidesmin producers. Enzyme-linked immuno-
sorbent assays and high-performance liquid chromatography
methods can be used to detect sporidesmin in body tissues
and grass.18,80 The differential diagnosis should be made with
plant poisoning that causes hepatic photosensitization,
mainly Brachiaria spp. and Panicum spp., which contain
lithogenic steroidal saponins and cause a disease similar to
pithomycotoxicosis. Histologically, the liver lesions induced
by saponin-containing plants are characterized by the pres-
ence of crystals in the bile ducts or within macrophages. The
presence of foamy macrophages in the liver is also a charac-
teristic of Brachiaria spp. poisoning.58 Poisoning by plants
such as Lantana spp., Myoporum laetum, Stryphnodendron
spp., Enterolobium spp., and Senecio spp. should also be
considered in the differential diagnosis.62
All ruminants must be removed from the infected pas-
tures. Affected animals should be placed in permanent
shadow with food and water and treated symptomatically if
necessary. These pastures should not be used again until their
conditions have changed or until the spore count demon-
strates a nontoxic fungal concentration. For prophylaxis,
pasture management practices should be used to prevent the
accumulation of dead plant matter. When these conditions
occur, the pastures can be monitored for toxicity by spore
counting. However, in countries where not all P. chartarum
strains are toxic, this practice can overestimate the risk of
poisoning.18 Reducing grazing pressure can also reduce toxin
intake, as the highest toxin levels are generally in those parts
of the pasture closest to the ground. In New Zealand, other
practices have been used to prevent facial eczema, including
dosing the animals with zinc salts to protect them against the
toxic effect of sporidesmin, spraying the pastures with fungi-
cides to reduce spore production, and breeding sheep or cat-
tle with increased resistance to the toxin.75 The substitution
of toxigenic strains of P. chartarum by nontoxigenic strains
was proposed in New Zealand as a way to control facial
eczema. Unfortunately, nontoxigenic strains, initially repre-
senting 80–90% of the isolates, did not persist in the pastures
and constituted only 4% of the strains after 4 months.80 How-
ever, survival of nontoxigenic strains may not be a problem
in South American countries where P. chartarum constitutes
a high percentage of the nontoxigenic strains.18
Diplodiosis
Diplodiosis is a mycotoxicosis caused by Stenocarpella
maydis (syn. Diplodia maydis) in cattle and sheep grazing
maize harvested fields. Stenocarpella maydis produce a thick
mass of mycelium in the cob, leaves, and stem of maize
(Fig. 4A), and after maturation, the fungi forms black,
pinhead-sized pycnidia (Fig. 4B).32,48,60 A substituted
β-cyclopropylamino acid toxin named diplonine was identi-
fied in S. maydis and found to cause nervous signs in guinea
pigs, similar to those observed in ruminants.76
Mycotoxicoses of ruminants and horses 9
Figure 4. Maize infected by Stenocarpella maydis (syn. Diplodia
maydis). A, fungus is forming a thick mass of mycelium. B, masses
of black pycnidia. Inset: pycnidia of S. maydis. Bar = 20 µm.
Diplodiosis is the most important mycotoxicosis of sheep
and cattle in southern Africa32 and has also been reported in
cattle in Brazil60 and Argentina48 in corn stubbles during the
autumn and winter (April–September). The morbidity rate is
5–75%, the mortality rate is 2–20%, and animals of different
ages are affected.60
Clinical signs in cattle include weeping, salivation, mus-
cle tremors, ataxia, and dysmetria with exaggerated flexion
of the limbs during gait. A wide-based stance and stiff gait
are also observed. Some animals become recumbent and
may develop opisthotonus and extension of the limbs. The
first clinical signs occur 2–10 days after consumption of
moldy maize. After being removed from stubble, the animals
recover in 7–10 days.48,60 Stillborns and neonatal mortality
can occur in pregnant cows and sheep without clinical signs
following the ingestion of contaminated corn.32 There are no
significant gross lesions. Histologically, spongiosis (status
spongiosus) of the cerebellar and cerebral white matter may
be observed in cases of long duration.32 In Argentina, moder-
ate to severe myelin degeneration has been observed in the
white matter of the cerebellum.48 Spongiosis has also been
observed in lambs and calves that die around the time of par-
turition.32
The diagnosis of diplodiosis must be established by the
observation of nervous signs in cattle grazing in corn stub-
bles during the winter. The main differential diagnosis is
with tremorgenic diseases caused by indole-diterpenoid
mycotoxins and with poisoning by Ipomoea asarifolia and
Phalaris spp. Poisoning by Aspergillus clavatus shares simi-
lar signs with diplodiosis but has a higher mortality rate. A
detailed histologic examination of the central nervous sys-
tem should help in the differential diagnosis, mainly in cases
of neonatal mortality when the dams do not show clinical
signs.
There is no specific treatment for diplodiosis. After the
observation of clinical signs, the herd must be removed from
the corn stubbles immediately. Because the pycnidia of the
fungus overwinter in the soil, maize residues should be
removed from the area (i.e., by deep early plowing or burn-
ing) to decrease contamination of the next crop. Alternating
maize cultures with other cultures can also help control corn
contamination by S. maydis.
Slaframine poisoning
Slaframine is an indolizidine alkaloid produced by the fun-
gus Rhizoctonia leguminicola, which infects leguminous
pastures, mainly Trifolium pratense (red clover or rotklee)
and Medicago sativa (alfalfa or lucerne).21 In the liver,
slaframine is metabolized to 6-ketoimine, which is similar
to acetylcholine. This active metabolite causes excessive
salivation and other parasympathomimetic effects.21 Rhi-
zoctonia leguminicola causes a disease called “blackpatch”
in leguminous plants, characterized by dark patches up to
1–3 mm in length on the leaves or stems (Gough FJ, Elliott
ES: 1956, Blackpatch of red clover and other legumes
caused by Rhizoctonia leguminicola sp. nov. Bulletin 387T,
West Virginia University Agricultural Experiment Station,
Morgantown, West Virginia. Available at: http://archive.org/
stream/blackpatchofredc387goug#page/n1/mode/2up). Rhi-
zoctonia leguminicola also contains swainsonine, which
may be responsible for some of the clinical signs observed
in the disease.21
Slaframine poisoning, known as slobbers, has been
reported in the United States and other countries and pri-
marily affects cattle and horses, although goats may also be
affected.21,82 In Uruguay (Riet-Correa F, et al.: 2007,
[Mycotoxicosis in grazing domestic animals]) and Argen-
tina,50 the disease has been observed in cattle grazing red
clover. In the Brazilian state of São Paulo, slobbers was
diagnosed in horses that ingested alfalfa hay, which was
produced in southern Brazil (state of Paraná) and stored for
4 months before consumption.8 In Uruguay and Argentina,
the disease has been reported to occur during the fall
(April–June), apparently as a result of excessive rainfall
(Riet-Correa F, et al.: 2007). Poisoning also occurs by the
ingestion of alfalfa or red clover hay, in which 5–10% of
the original toxicity remains after 10 months.21
In cattle, clinical signs are decreased milk production,
salivation, lacrimation, and piloerection. Some animals may
show frequent urination, stiff gait, dyspnea, bloat, and
Riet-Correa et al.
10
increased frequency of defecation (Riet-Correa F, et al.:
2007, [Mycotoxicosis in grazing domestic animals]).50
Horses show light to intense drooling accompanied by con-
stant movement of the tongue.8 Salivation appears 5–6 hr
after ingestion of the contaminated food, and the animal
recovers 24 hr after removal of the contaminated diet. A pre-
sumptive diagnosis can be made by the observation of saliva-
tion in animals ingesting leguminous pastures or hay.
Rhizoctonia leguminicola poisoning can be confirmed by
microscopic observation or fungal isolation from the typical
black spots on the plants. To detect slaframine activity, pas-
tures, hay, or their extracts can be administered to guinea
pigs to induce salivation. The toxin can be identified by gas
chromatography and mass spectrometry. The differential
diagnosis includes vesicular stomatitis and salivation in indi-
vidual horses caused by choking, oral trauma, oral foreign
bodies, dental problems, glossitis, and treatment with the
drug imidocarb, which causes salivation by reversible inhibi-
tion of cholinesterase.8 In cattle, the main differential diag-
nosis is with foot and mouth disease and vesicular or
ulcerative stomatitis. Affected animals may be treated with
atropine to reduce the salivation.50 There is no practical way
to control R. leguminicola in the pastures or hay, but seeds
can be treated with fungicides to avoid transmission to
fungus-free areas (Gough FJ, Elliott ES: 1956, Blackpatch of
red clover and other legumes).
Aflatoxicosis
Aflatoxins are a group of hepatotoxic metabolites (primar-
ily aflatoxins B1, B2, G1, and G2) produced by some
strains of Aspergillus, mainly A. flavus and A. parasiticus,
at temperatures of 24–35°C and humidity greater than
14%.43,49 Aflatoxin B1 is biotransformed by liver micro-
somal mixed-function oxidases to form several metabo-
lites, including aflatoxin B1-8,9-epoxide that binds
covalently to nucleic acids and proteins and seems to be
responsible for cellular necrosis, immune suppression,
mutagenesis, and neoplasms.43,49 Aflatoxicosis is a disease
that predominantly affects animals that ingest grains or
grain byproducts. Pigs and poultry are most often affected,
but aflatoxicosis can also occur in other species including
cattle (Lafluf O, Termezana A, Rivero R, et al.: 1989, Un
caso de aflatoxicosis en bovinos asociado a maíz carbonoso
[A case of aflatoxicosis associated with corn infected by
Ustilago maydis]. Buiatrics Uruguayan XVII Conference,
Paysandú, Uruguay, sección cc8, pp. 1–8).25,40,51 Young ani-
mals are more susceptible than adults, and, in cattle, the
disease is more common in calves and dairy cows than in
adult beef cattle. Aflatoxins only cause clinical signs in
calves at high doses (e.g., 0.02–0.08 mg of aflatoxin B1 per
kg of body weight daily).52 However, the effects of afla-
toxin poisoning in cattle depend on the aflatoxin concentra-
tion in the food, the length of the feeding period, and the
age of the animals. In horses, aflatoxicosis is a rare
disease,49 and the few reported cases have been reviewed.13
As in other species, aflatoxicosis in horses affects mainly
the liver causing hepatocellular degeneration, necrosis, and
megalocytosis, as well as bile duct proliferation and fibro-
sis. Hemorrhagic enteritis and pale kidneys with protein
precipitate in renal tubules are also observed.13,49 An out-
break of aflatoxicosis was reported in young goats follow-
ing ingestion of polkudu meal (defatted residue from grated
coconut after juice extraction),73 and decreased milk pro-
duction has been reported in goats following aflatoxin
ingestion.28 Sheep are resistant to aflatoxins, although high
concentrations (2,000 ppb) have been associated with a
decrease in weight gain.25
In Uruguay, an outbreak of aflatoxicosis occurred in cattle
that had been grazed for 2 weeks in a corn field in which corn
was not harvested due to heavy infection by Ustilago may-
dis. Out of 81 Holstein dairy cows, 10 became ill and 3 died.
Aspergillus flavus was isolated from the corn, which was
found to contain 2,700 ppb of aflatoxin B1. The poor condi-
tion of this corn, due to U. maydis infection, favored the
development of the toxigenic strains of this fungus. High
infection by this fungus occurs when rainfall is scarce during
the vegetative period of the plant (Lafluf O, et al.: 1989, [A
case of aflatoxicosis]). In Uruguay and Brazil, outbreaks of
aflatoxicosis were reported in steers that had ingested a
ration constituted by 70% sorghum wet grain silage and 27%
sorghum silage containing 20 ppb of aflatoxins25 and in
4-month-old calves that ingested a ration that consisted of
alfalfa hay, broken corn, and milk substitute containing 5,136
ppb of aflatoxin B1.51 The mortality rates varied from 1.6%
to 15%.25,51
The most frequent clinical signs of chronic aflatoxicosis,
caused by ingestion of aflatoxins for weeks or months, are
a decrease in milk production in dairy cattle and lower
weight gains in growing animals. Some animals show signs
of liver failure, including general unthriftiness, rough coats,
anorexia, depression, food refusal, abdominal pain with
colic, grinding of the teeth, photosensitivity, severe diar-
rhea, and rectal tenesmus, sometimes with a prolapsed rec-
tum.20,51 Acute aflatoxicosis is rare, but has been reported to
cause anorexia, depression, jaundice, photodermatitis, sub-
mandibular edema, diarrhea (sometimes bloody), nervous
signs, and abortion (Lafluf O, et al.: 1989, [A case of afla-
toxicosis]).40 Most likely, the most important form of afla-
toxicosis is subclinical and nonspecific, causing reduced
milk production, lower weight gains, and immune depres-
sion associated with an increased frequency of diarrhea,
respiratory disease, and mastitis. The increased serum
activities of alkaline phosphatase and gamma-glutamyl
transpeptidase are good indicators of liver damage due to
aflatoxins.52
Gross lesions include color changes and increased consis-
tency of the liver, gall bladder dilatation with wall edema,
and edema of the mesentery and wall of the abomasum
(Lafluf O, et al.: 1989, [A case of aflatoxicosis]).20,40 In acute
Mycotoxicoses of ruminants and horses 11
cases, there may be jaundice and bleeding of the subcutane-
ous tissue, skeletal muscles, lymph nodes, pericardium, and
gastrointestinal tract (Lafluf O, et al.: 1989).40 Histological
changes of the liver are characterized by periportal fibrosis,
bile duct cell proliferation, megalocytosis, and vacuolization
or single-cell necrosis of hepatocytes (Lafluf O, et al.:
1989).20,40,51
The presumptive diagnosis of aflatoxicosis is made
through epidemiological data, clinical signs, gross lesions,
and primarily by the presence of histological lesions. The
definitive diagnosis should rely on the detection of aflatoxins
in the food and the characteristic histologic lesions. How-
ever, it should be noted that the aflatoxin analysis of the
sample is not representative of food consumed during the
previous weeks or months and that histologic lesions are not
specific. The main differential diagnosis is with poisoning by
plants containing pyrrolizidine alkaloids (Senecio spp.,
Echium plantagineum, Erechtites hieracifolia, and Crota-
laria spp. in South America). In feedlots, hay or silage should
be observed to detect the possible presence of these plants.
Crops can be contaminated by Crotalaria spp. seeds. In the
subclinical form, other diseases and management mistakes
that cause reduced production and impaired immunity should
be considered.
For control of aflatoxicosis, the contaminated food
should be immediately removed from the diet. For preven-
tion, it is important to avoid feeding animals any crops or
byproducts that have been stored improperly. Surveying
feed crops for the presence of aflatoxins is the best way to
prevent aflatoxicosis, especially the subclinical form. Alu-
minosilicate products such as hydrated calcium alumino-
silicate and sodium bentonite, which are effective in binding
aflatoxins and preventing their absorption, have been
widely used in the pig and poultry industries to prevent
aflatoxicosis.
Poisoning by Aspergillus clavatus
Poisoning by Aspergillus clavatus leads to neuromycotoxi-
cosis of cattle and sheep, characterized by tremors, ataxia,
weakness, paresis, and recumbence followed by death. This
poisoning occurs primarily in animals that ingest malting
residues contaminated with A. clavatus.32,37,55,72,74 In Brazil,
this neuromycotoxicosis was reproduced in cattle19 and
sheep4 fed corn contaminated with A. clavatus, which pro-
duces several toxic metabolites, including patulin, trypto-
quivalines, cytochalasin E, and glyantripine.55,72 Aspergillus
clavatus poisoning has also been reported in animals that
have ingested sprouting wheat, sprouting maize, and sor-
ghum beer residues.32 In Uruguay, the disease was also
reported in cattle that ingested sugar beet residues, which
were widely used as animal feed in that country until the
1980s. Toxigenic strains of A. clavatus were isolated from
toxic sugar beet residues stored under humidity and tempera-
ture conditions suitable for fungal growth.55
The morbidity rates of poisoning by malting residues
varied between 17% and 32%, and mortality ranged from
25% to 87%.19,55 In cases of poisoning by sugar beet resi-
dues, morbidity rates were 35–93%, and mortality rates
were 8.6–34.4%.
Clinical signs include instability, ataxia, weakness or
paralysis mainly of the hind limbs, and an inability to rise
(Fig. 5A, 5B). Initially, affected cattle appear normal at rest,
but manifest clinical signs when stimulated. If the animals
are exercised or forced to move, they display muscle trem-
ors, and fall down into a position of sternal recumbence, fre-
quently with the legs extended or in a dog-sitting position.
After a short rest, some animals rise and walk normally, but
others stay recumbent and may present mild head tremors,
salivation, and loss of spinal cord reflexes. Lateral recum-
bence and paddling are observed in the terminal phase.37 The
clinical course of the disease varies from 2–3 days to 2
weeks. Deaths occur during a period of several weeks. The
morbidity rate is 17–32%, and the mortality rate is 25–
87%.19,55 A mortality rate of 97% has been reported in
sheep.74
The main gross lesion is a whitish appearance of the
large muscles of the fore and hind limbs (Fig. 5C). His-
tologically, severe chromatolysis, paleness, vacuolation,
and margination of the nuclei occur in the neurons of the
midbrain, medulla oblongata, and pons and in the ventral
horn of the spinal cord (Fig. 5D).37,72 Axonal degenera-
tion is observed in the white matter of the central ner-
vous system and in the peripheral nerves.72 Focal
degeneration and necrosis are present in the skeletal
muscles.
The presence of the histologic lesions described above
and a history of feeding with barley or sugar beet residues
are the most important criteria for the diagnosis of A. clava-
tus poisoning. Aspergillus clavatus can be isolated from the
food, but it is important to consider that not all strains are
toxigenic. Multitoxin and patulin analysis of the contami-
nated food and isolation of A. clavatus should be performed
to confirm the diagnosis. The main differential diagnoses
are poisoning by indole-diterpenoid mycotoxins and botu-
lism. Indole-diterpenoid poisoning is a tremorgenic disease
with much lower mortality rates, and the animals recover in
a few days after withdrawal of the contaminated food. Clin-
ically, botulism is very similar to A. clavatus poisoning, but
in the latter, neuronal lesions do not occur and muscle
lesions are much less common. Analysis for botulism toxin
in more than 1 animal is important for diagnosis. In South
America, paralytic rabies transmitted by bats causes a simi-
lar disease, but with 100% fatality and typical histologic
lesions.
In cases of A. clavatus poisoning, the contaminated food
should be removed from the diet immediately. To prevent
poisoning, barley, barley residues, or beet residues should be
stored under appropriate environmental conditions to avoid
fungal contamination.
Riet-Correa et al.
12
Poisoning by moldy sweet potatoes
(Ipomoea batatas)
Sweet potatoes (Ipomoea batatas) infected by Fusarium
solani (Fig. 6A) may contain 3-substituted furans, including
4-ipomeanol, 1-ipomeanol, 1,4-ipomeadiol, and ipomeanine,
which cause acute respiratory distress in cattle. This disease
is not technically a mycotoxicosis because the toxins are pro-
duced by the tubercle after it has been infected by the fungi.
Fusarium solani stimulates host tissues to form ipomeama-
rone and 4-hydroxymyoporone; the latter is then converted
to 4-ipomeanol, 1-ipomeanol, and 1,4-ipomeadiol.62 Other
fungi, including Fusarium oxysporum, have been isolated
from sweet potatoes in some outbreaks.26,41 Mechanical
injury, chemical treatments, and parasitic infections can
also induce the production of 3-substituted furans by sweet
potatoes. In some regions, animals are commonly fed
tubercles that are visibly moldy (Fig. 6A) or infected by
parasites, as these potatoes are considered unfit for human
consumption.26,41
Poisoning has been reported in Brazil26,41 and Uruguay.69
The clinical signs include severe respiratory distress with
dyspnea, coughing, salivation, and dilated nostrils. Greatly
affected animals adopt a position with an extended neck and
hanging head. The clinical manifestation period varies from
3–5 days.26,41,69 Necropsy lesions include distended and pale
lungs with a rubbery consistency that does not collapse when
the thorax is opened. Pulmonary edema and emphysema
(Fig. 6B), as well as white foam, can also be observed in the
airways. Sweet potato residues can be found in the rumen
content. Histologically, the interlobular septa and the sub-
pleural tissues are distended by edema and emphysema (Fig.
6C). Additional signs are thickening of the alveolar walls by
inflammatory cells and edema. The alveoli can be lined by
type II pneumocytes, and the pulmonary lymphatic vessels
are dilated by air.26,41 The clinical signs and pathology, as
well as a history of feeding moldy sweet potatoes, usually
allow diagnosis of this type of poisoning, and the macro-
scopic and histological lesions are characteristic. However,
there are several causes of interstitial pneumonia, grouped
under the name “atypical interstitial pneumonia,” including
poisoning by d-tryptophan and/or l-tryptophan in pastures,
poisoning by Perilla frutescens, inhalation of irritant gasses,
and lungworm infestation; all of these should be considered
in the differential diagnosis because they produce clinical
signs and lesions similar to those observed in poisoning by
Figure 5. Poisoning by Aspergillus clavatus. A, B, cattle poisoned by A. clavatus toxins showing weakness of the hind limbs and
recumbence. C, whitish appearance of the hind limb muscles due to degeneration and necrosis. D, chromatolysis and cytoplasmatic pallor
with cellular swelling of neurons is observed in the brain. Hematoxylin and eosin. Bar = 100 µm. Photos courtesy David Driemeier, Pedro
Bezerra, and Alexandre Loretti.
Mycotoxicoses of ruminants and horses 13
moldy sweet potatoes. To prevent this type of poisoning, it is
necessary to avoid feeding the animals with sweet potatoes if
the storage conditions are not suitable and the tubercles are
contaminated by fungi or parasites.
Leukoencephalomalacia
Leukoencephalomalacia (LEM) is a disease of equids caused
by ingesting moldy corn contaminated by the fungus of the
genera Fusarium, including Fusarium verticillioides (syn. F.
moniliforme) and Fusarium proliferatum, which produce
fumonisin. Many fumonisins have been identified, but only
fumonisins B1 and B2 are important as a cause of LEM.
Fumonisins alter sphingolipid metabolism by inhibiting
ceramide synthase, an important enzyme in the biosynthesis
of sphingolipids. High doses of fumonisin B1 may cause
hepatotoxicity. In Brazil, F. verticillioides has been isolated
consistently from samples of corn that cause LEM.2,29,64,83
Fusarium proliferatum and Fusarium subglutinans are less
frequently isolated. Levels of fumonisin B1 ranging from 10
to 500 µg/g were detected in 24 samples of corn that caused
LEM.63 In another 13 samples, fumonisin B1 concentrations
ranged from 0.2 mg/g to 38.5 mg/g, and fumonisin B2 con-
centrations were between 0.1 and 12 µg/g.79 In Argentina,
fumonisin B1 and B2 concentrations were 12.5 and 5.2 µg/g,
respectively, in a feed supplement that caused LEM.27
Leukoencephalomalacia has been diagnosed in horses in
all regions of Brazil,2,12,29,53,63,64,67,79,83 in Argentina27,42 and
Uruguay,68 and in mules in the Brazilian states of Pernam-
buco and Pará.14,67 Outbreaks occur in animals that are fed
corn kernels, corn cobs, ground whole corn (a mixture of
corn, corn stalks, and corn cobs), corn bran, corn screenings,
or other byproducts from the processing of corn for human
consumption. Corn that causes LEM may not be visibly
moldy. Some outbreaks are caused by apparently normal
corn contaminated by F. verticillioides. In the southern and
southeastern regions of Brazil, LEM is seasonal, occurring
mainly between June and September, although outbreaks
have been recorded from March to December.2,63,64 In tropi-
cal climates, outbreaks occur in both the dry and rainy sea-
sons.14,67 Fusarium verticillioides infection of maize is more
frequent when periods of drought are followed by cool, wet
weather during pollination.43
In corn samples from 21 outbreaks of LEM, the moisture
was 16.98 ± 2.30%. In 5 samples, the moisture was below
15%, which is in accordance with Brazilian standards for
corn storage.63 In outbreaks reported in southern Brazil,
LEM occurred in horses ingesting more than 1 kg of corn
daily or rations containing more than 20% corn.63 Animals of
different ages and both sexes can be affected. Morbidity rates
are 4–100%, and case fatality rates are nearly 100%.27,63,68
Partial recovery has been reported in some cases,27 although
this is rare.
Clinical signs of LEM appear abruptly and are character-
istic of lesions of the cerebrum and brain stem, including
anorexia, dullness, drowsiness, occasional hyperexcitability,
muscle tremors, compulsive walking, head pressing, cir-
cling, chewing difficulties, unilateral or bilateral blindness,
ataxia, decreased eyelid reflex, decreased tone of the tongue
and lips, loss of sensitivity of the face, paralysis of the jaw,
and recumbence.2,12,27,63,64,67 The clinical manifestation
period is 2–72 hr, but most affected animals die within 6–24
hr. Occasionally, the clinical course may last up to 13 days.
In some outbreaks, the clinical signs may appear up to 12
days after the corn is withdrawn from the diet.
The lesions are almost bilateral, but asymmetric, with one
side much more affected than the other and are located in the
Figure 6. Poisoning by moldy sweet potatoes (Ipomoea bata-
tas). A, moldy sweet potatoes. B, lung with emphysema and edema.
C, histologic section of the lung showing severe alveolar and inter-
stitial emphysema. Hematoxylin and eosin. Bar = 100 µm.
Riet-Correa et al.
14
cerebrum and/or brain stem. One of the cerebral hemispheres
may be enlarged, and malacia of the white matter may be
observed on the cut surface, with multifocal to coalescing
foci of hemorrhage, brown-yellow discoloration, and soften-
ing of the centrum semiovale and corona radiata (Fig. 7A).
Cavities containing fluid are often observed in these areas.
The internal capsule and thalamus are usually affected, but
lesions may be observed also in the mesencephalon (Fig. 7B),
cerebellar peduncles, pons, and medulla oblongata. The
macroscopic lesions are better evidenced after fixation of the
central nervous system in 10–25% formalin, but cavitation,
edema (yellow areas), and hemorrhages are easily observed
in fresh brain tissue (Fig. 8). In some horses, the liver may be
enlarged and yellowish.2,12,63,64,67,83
Histologically, malacia surrounded by edema and hemor-
rhage of the neuropil are observed (Fig. 9). An additional
characteristic of LEM is the presence of swollen astrocytes
or oligodendrocytes, with abundant eosinophilic cytoplasm,
deeply eosinophilic intracytoplasmic globules, and eccentric
hyperchromatic nuclei (Fig. 9).14,27,63,67 These cells, previ-
ously known as clasmatodendritic astroglia, are found in
areas of hemorrhage and edema and are swollen because
they have imbibed plasma protein. Additional lesions include
hypertrophic and degenerative changes in the vascular endo-
thelium and perivascular edema, hemorrhages, and eosino-
philic globules. Some vessels have perivascular cuffing of
eosinophils, neutrophils, or mononuclear cells.2,12,63,64,67,83
Figure 7. Leukoencephalomalacia in equid. A, a formalin-
fixed cerebrum showing yellow areas of edema, hemorrhages, and
cavitation of the white matter. Photo courtesy Dr. Jose A. B. da Silva
and Ciência Animal Brasileira. B, formalin-fixed mesencephalon
showing cavitation and hemorrhages.
Figure 8. Leukoencephalomalacia in equid. Fresh cerebrum
showing enlarged left hemisphere with hemorrhages (arrows) and
yellow discoloration of the white matter (*).
Figure 9. Equine leukoencephalomalacia; cerebral white mat-
ter. Malacia (M), perivascular edema (E), and hemorrhages (H) and
numerous characteristic reactive glial cells with abundant eosino-
philic cytoplasm, sometimes called clasmatodendritic astroglia, are
observed (arrows). Hematoxylin and eosin (HE). Bar = 100 µm.
Inset: reactive glial cells (arrows). HE. Bar = 30 µm.
Mycotoxicoses of ruminants and horses 15
Affected horses may also have hepatic lesions, including
vacuolization or necrosis of the hepatocytes.
The diagnosis of LEM is based on the occurrence of the
disease in horses that have ingested diets containing corn or
corn byproducts. The main differential diagnosis is with
rabies, viral equine encephalitis, and hepatic encephalopathy,
which is caused primarily by poisoning with pyrrolizidine
alkaloids. Malacia of the white matter, macroscopically simi-
lar to that caused by LEM, is observed in equine trypanoso-
miasis caused by Trypanosoma evansi. In trypanosomiasis,
however, the main histologic lesion is severe encephalitis,
and the clinical manifestation period is much longer. The only
way to prevent LEM is to avoid the ingestion of improperly
dried corn. When the corn is properly dried, it should not con-
stitute more than 20% of the dry matter.
Declaration of conflicting interests
The author(s) declared no potential conflicts of interest with respect to
the research, authorship, and/or publication of this article. [AQ: 2]
Funding
The author(s) disclosed receipt of the following financial support
for the research, authorship, and/or publication of this article: This
work was supported by National Institute for Science and Technol-
ogy for the Control of Plant Poisonings, National Council of Scien-
tific and Technological Development (CNPq; grant 573534/2008-0).
[AQ: 3]
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