Research in Veterinary Science 93 (2012) 1337–1340

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Research in Veterinary Science

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Primary photosensitization in cattle caused by Froelichia humboldtiana

Paulo E.C. Souza a, Samuel S. Oliveira b, Cristiano R. Aguiar-Filho b, Ana L.B. Cunha b, Raquel F. Albuquerque a,Joaquim Evêncio-Neto a, Franklin Riet-Correa c, Fábio S. Mendonça a,⇑a Departamento de Morfologia de Fisiologia Animal, UFRPE, Recife PE 52171-900, Brazilb Departamento de Medicina Veterinária, UFRPE, Recife PE 52171-900, Brazilc Hospital Veterinário, CSTR, UFCG, Campus de Patos, Patos PB 58700-000, Brazil

a r t i c l e i n f o

Article history:Received 22 November 2011Accepted 8 April 2012

Keywords:PhotodermatitisPlant poisoningPoisonous plantsBovines

0034-5288/$ - see front matter � 2012 Elsevier Ltd. Ahttp://dx.doi.org/10.1016/j.rvsc.2012.04.005

⇑ Corresponding author. Tel.: +55 81 33206387; faxE-mail address: mendonca@dmfa.ufrpe.br (F.S. Me

a b s t r a c t

Three outbreaks of primary photosensitization caused by Froelichia humboldtiana are reported in thesemiarid region of the states of Pernambuco and Paraíba, in northeastern Brazil. The disease occurredfrom March to June 2011, affecting 27 bovines out of a total of 70. The main lesions consisted of derma-titis of the white skin, with edema and necrosis. All the bovines recovered after removal from the areasinvaded by F. humboldtiana. To produce the disease experimentally, one bovine with white skin wasplaced for 14 days into an area with F. humboldtiana as the sole forage. This bovine presented photoder-matitis on the third day of consumption. The serum concentrations of total, indirect, and conjugated bil-irubin and the serum activities of gamma-glutamyl transferase (GGT) and aspartate-aminotransferase(AST) in the spontaneously affected cattle and in the experimental cattle remained within normal ranges.It is concluded that F. humboldtiana causes primary photosensitization in cattle in northeastern Brazil.

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Froelichia humboldtiana (Roem. & Schult.) (Amaranthacea), com-monly known in Portuguese as ervanço, is a plant widely distrib-uted in the Brazilian northeastern region and also found in someareas of central-western Brazil (Marchioretto et al., 2002).

Outbreaks of photosensitization affecting horses are wellknown in the semiarid northeastern region of Brazil, where farm-ers claimed that the disease also affects mules, donkeys, sheep,and cattle (Macedo et al., 2006; Pimentel et al., 2007). After a spon-taneous photosensitization outbreak in sheep, the poisoning wasexperimentally produced in 4 sheep and in a foal grazing in a re-stricted area with F. humboldtiana as the sole vegetation (Pimentelet al., 2007).

The aim of this study is to report primary photosensitization incattle in the semiarid region of Brazil and to demonstrateexperimentally that the disease is caused by the ingestion ofF. humboldtiana.

The epidemiologic and clinical data were obtained from ownersand veterinarians during visits to the farms in which the diseasewas occurring. The climate in the region is semiarid, the annualrainfall average is 450 mm, and the vegetation consists of Braziliancaatinga, a biome exclusive to Brazil that is characterized bybushes with twisted branches and deep roots, cacti and bromeliads(Costa et al., 2007). In the three farms studied, 12 cattle naturallypoisoned by F. humboldtiana were examined, and samples of theirperipheral blood were collected to analyze the serum activities of

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gamma-glutamyl transferase (GGT) and aspartate-aminotransfer-ase (AST), and the serum concentrations of the total, indirect, andconjugated bilirubin (Kaneko et al., 1997).

In one farm in the municipality of Custódia in the state ofPernambuco, 4 cattle out of 18 presented photodermatitis lesionsafter being kept for 10 days in a newly established grazing areaof approximately 3 hectares. The disease occurred from March toMay 2011, during the rainy season (Fig. 1), and affected cattleraised in a semi-extensive system. The grazing area was originallycovered by the Brazilian caatinga, and buffel grass (Cenchrusciliares) was later planted, but the planting was not successful,and the area was severely invaded by F. humboldtiana (Fig. 2).

Other outbreaks of photodermatitis affecting cattle were alsoobserved in two farms in the municipality of Salgado de São Félix,in the state of Paraíba. Twenty-three bovines out of a total of 52 atrisk were affected. One 6-month-old calf died as a result of severephotodermatitis. The outbreaks occurred between May and July,also during the rainy season (Fig. 1). The cattle were free to grazein the early morning in areas of approximately 5 hectares and wereremoved in the late afternoon. In both farms, an intense invasion ofthe paddocks by F. humboldtiana was observed.

The plant is highly palatable, and animals consume largeamounts of it. According to the farmers, the disease occurs season-ally during the rainy season when the plant is flowering. Cattle andhorses with non-pigmented white skin are more frequently af-fected, but goats and sheep are also affected. The farmers men-tioned that cattle purchased from other regions have moresevere lesions of photodermatitis than cattle born on the farms.

Fig. 1. Monthly rainfall in the municipality of Custódia, state of Pernambuco andSalgado de São Félix, state of Paraíba in 2011 (rainy season). Data from the Brazilianagencies IPA and EMATER.

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The cattle naturally poisoned were in good physical condition,and lesions were observed in the areas of white skin (Fig. 3) or de-void of hairs. These animals were restless, scratching themselves,often seeking shaded areas, and constantly licking the areas of in-jury. Dermatitis with alopecia affected mainly the outside of theears and around the eyes, the forehead, the nose, the muzzle, thedorsal portion of the neck, the croup, the withers, the scrotum,the teats, and the perineal region. The most severe lesions showedalopecia, edema, crusts and skin necrosis (Fig. 3). The serum activ-ities of the GGT and AST and the serum concentrations of bilirubinin the naturally affected cattle remained normal according to theparameters for the species (Kaneko et al. 1997).

After diagnosis of the poisoning, the herds were removed fromthe pastures invaded by F. humboldtiana and clinically evaluatedafter 30 and 90 days. The animals with lesions of less than approx-imately 8 cm in diameter recovered within 30 days. In the bovineswith larger and more severe lesions, the lesions took up to 90 daysto heal.

Additionally, to study the epidemiology of the disease, 9 otherneighboring farms were visited. In the 9 farms, the farmers also re-

Fig. 2. (A) Pasture heavily infested by Froelichia hu

ported the occurrence of the disease in horses, cattle, goats, andsheep associated with the presence of F. humboldtiana.

To produce the disease experimentally, one 3-year-old Holsteincrossbreed cow with areas of white skin was kept for 14 days in apasture severely invaded by F. humboldtiana. This cow came from aregion where F. humboldtiana was not present. The experiment wasperformed in April, during the rainy season. In the area where theexperimental animal was grazing, other plants were manually up-rooted to be sure that the only plant ingested was F. humboldtiana.At night, the cow was removed to the corral where it remainedwithout access to other food. The experimental cow was examineddaily for the presence of photodermatitis. Samples of its peripheralblood were collected on the 1st and 14th days of the experiment toanalyze the serum activities of the GGT and the AST and the serumconcentrations of the total, indirect and conjugated bilirubin. Twoother 8- and 12-month-old cattle with areas of white skin wereused as controls. During the day, these animals were maintainedin a paddock of approximately 1 hectare where there was no F.humboldtiana. They were removed to the corral at night.

On the third day after being placed in the pasture with the F.humboldtiana, the cow was restless and scratched itself frequently.Later, hyperemia and photodermatitis were observed affecting theforehead, the dorsal portion of the neck, the withers, and the prox-imal hind limbs. On the 12th day of the experiment, alopecia, cuta-neous edema, and skin necrosis were also observed. The lesionsregressed gradually after the removal of the cow from the paddock,and complete healing of all the lesions occurred without treatmentin 45 days. There were no changes in the serum activities of theGGT and the AST and in the serum bilirubin concentrations.

The diagnosis of poisoning and primary photosensitization by F.humboldtiana was based on epidemiology, clinical signs, serumbiochemistry and the experimental reproduction of the disease.In the spontaneous and experimental cases, the serum activitiesof the GGT and the AST and the serum concentrations of bilirubinremained within normal limits, demonstrating that the photosen-sitization was primary and not secondary to liver disease.

Polyphenolic pigments present in some plants cause primaryphotosensitization. After ingestion, these pigments are absorbedby the digestive tract and distributed by the bloodstream. In ani-mals with non-pigmented skin, these compounds react rapidlywith UV rays, producing cell death and tissue necrosis in the epi-dermal cells (Knight and Walter, 2001).

mboldtiana. (B) Aerial part of F. humboldtiana.

Fig. 3. Cattle naturally poisoned by Froelichia humboldtiana. Dermatitis with alopecia, edema, crusts, and skin necrosis is observed mainly in the white skin of the flank (A),lumbosacral region (B and D) and teats (C).

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Plants causing primary photosensitization in ruminants includeFagopyrum esculentum and Hypericum perforatum, which containphotodynamic naphthodianthrones: fagopyrin in the F. esculentum(Kingsbury, 1964) and hypericin in the H. perforatum (Marsh, 1930;Sampson and Parker, 1930; Araya and Ford, 1981). Ammi majus(Dollahite et al., 1978), Thamnosma texana (Oertli et al., 1983),Cymopterus watsonii (Stermitz and Thomas, 1975) and Cooperiapedunculata (Rowe and Norman, 1989; Casteel et al., 1988) alsocause primary photosensitization, but due to another photody-namic compound called furocoumarins. Within these furocouma-rin-containing plants, A. majus is the only plant reportedpreviously in Brazil as a cause of primary photosensitization in cat-tle (Méndez et al., 1991). The toxin responsible for the photoder-matitis in F. humboldtiana is unknown. Based on the absence ofocular lesions in the affected animals, it is suggested that this plantcould contains naphthodianthrones or similar substances. Ocularlesions had not been reported in animals poisoned by plants con-taining naphthodianthrones, as they are observed in poisoning bysome plants containing furocoumarins (Pimentel et al., 2007).However, the polyphenolic compound 3,4-dihydroxyphenyl caff-eate was identified in Froenlichia floridana (Wang et al., 2009). Thissubstance is also found in A. majus (Hehmann et al., 2004).

Poisoning by F. humboldtiana is a well-known cause of economiclosses for horse breeders in the semiarid region of Brazil (Pimentelet al., 2007). However, according to the results of this study, thedisease is also important for cattle. Sheep and goats are apparentlyless frequently affected, but these data should be interpreted withcaution; poisoning is locally recognized by farmers and many casesmay not be reported.

Further studies should be conducted to determine the toxiccompound of the plant, the period in which it is more toxic, andif native cattle are more resistant to the poisoning than naïve

cattle. For the prophylaxis of the poisoning, it is necessary to avoidthe introduction of animals, mainly those with white skin, intoareas severely invaded by the plant.

Acknowledgment

We thank the Dean of Research from the Federal Rural Univer-sity of Pernambuco for its logistic support.

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