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Fotossensibilização Rumi e Eq Silvio
Fotossensibilização Rumi e Eq Silvio
Toxicon
journal homepage: http://www.elsevier.com/locate/toxicon
A R T I C L E I N F O A B S T R A C T
Handling Editor: Kevin Welch This study aimed to describe the first reports of outbreaks of hepatogenous photosensitization in cattle, sheep,
and horses caused by spontaneous ingestion of Chamaecrista serpens, as well as to reproduce poisoning in sheep
Keywords: experimentally. Eleven photodermatitis outbreaks of unknown cause occurred in cattle, sheep and horses on nine
Chamaecrista serpens farms in the semiarid region of Bahia, northeastern Brazil, between July 2017 and July 2020. Cutaneous lesions
Hepatogenous photosensitization
of photosensitization initiated until one week after the animals were introduced in paddocks invaded by the plant
Hepatotoxic plants
at the beginning of the rainy season. The photosensitive skin lesions were progressive and consisted of hyper
Photodermatitis
emia, edema, ulcerative-crusted lesions with necrosis, especially in non-pigmented skin areas. The lesions in
young animals were more severe. The animals avoided the sun and exhibited hyporexia, weight loss, restlessness,
irritability, and severe itching. An experimental study was made using seven sheep, and resulted in photo
dermatitis, similar to that observed in the natural poisoning, seven days after the beginning of plant ingestion.
Two sheep were reserved for the control group. Serum biochemistry changes indicated liver injury caused by the
plant. Skin biopsies and liver biopsy guided by ultrasound were performed. The one sheep that had more pro
nounced skin lesions was euthanized and necropsied. At the necropsy, the liver was enlarged, diffusely pale, and
firm, with an evident lobular pattern and an empty gallbladder. Histopathology revealed similar skin and liver
lesions in samples from biopsies and the necropsy. There was a marked disorganization of the cords of hepa
tocytes associated with degenerative necrotic changes on the liver. The cutaneous injuries included orthoker
atotic hyperkeratosis, hypergranulosis, acanthosis, and extensive areas of epidermic necrosis and ulceration.
Three sheep were protected from sunlight and the lesions regressed within 45 days after the plant’s consumption
ceased. In conclusion, C. serpens causes hepatogenous photosensitization in ruminants and horses, and should be
included in the list of differential diagnoses in cases of photosensitive dermatitis.
* Corresponding author.
E-mail addresses: mucinhoferraro@hotmail.com (M.F.F. Mendonça), lucianoanp@yahoo.com.br (L.A. Pimentel), paulavleal15@gmail.com (P.V. Leal),
jcoliveirafilho@ufrb.edu.br (J.C. Oliveira Filho), lais_caymmi@hotmail.com (L.G. Caymmi), antoniowesley_vet@hotmail.com (A.W.O. Silva), rubenssilva.agro@
gmail.com (R.S. Jesus), tcpeixoto@ufba.br (T.C. Peixoto).
https://doi.org/10.1016/j.toxicon.2021.01.013
Received 1 September 2020; Received in revised form 29 December 2020; Accepted 20 January 2021
Available online 28 January 2021
0041-0101/© 2021 Elsevier Ltd. All rights reserved.
M.F.F. Mendonça et al. Toxicon 193 (2021) 13–20
ingestion of Brachiaria spp. (Brum et al., 2009; Albernaz et al., 2010; trauma, erythema, edema, desquamation, necrosis, shedding of the
Souza et al., 2010; Faccin et al., 2014; Pupin et al., 2016), Enterolobium skin in the most affected parts, ulcerations, and crusting, as well as
contortisiliquum (Grecco et al., 2002; Olinda et al., 2015; Leal et al., restlessness, hyporexia, weight loss, and eventually death (Rowe, 1989;
2017), Stryphnodendron fissuratum (Ferreira et al., 2009; Lazaro et al., Tokarnia et al., 2012; Knupp et al., 2014; Constable et al., 2017).
2018), Lantana spp. (Rissi et al., 2007), Panicum spp. (Riet-Correa et al., In several municipalities of Bahia northeastern semiarid regions of
2009), and Crotalaria retusa (Lucena et al., 2010). Primary photosensi Brazil, farmers attribute cases of photosensitization in cattle, sheep,
tization is associated with poisoning from Ammi majus (Méndez et al., goats, and horses to spontaneous ingestion of Chamaecrista spp. How
1991), Froelichia humboldtiana (Pimentel et al., 2007; Silva Filho et al., ever, until now, there has been no scientific proof of this plant’s toxicity.
2020), and recently, Malachra fasciata (Araújo et al., 2017). Chamaecrista serpens (L.) Greene is a subshrub of the Fabaceae fam
Regardless of the cause, affected animals develop skin lesions pre ily, which is native to Brazil (Neto, 2010), occurring in most states apart
dominantly involving non-pigmented regions with less hair or wool from those in the west and south of the country (Souza and Bortoluzzi,
covering or those areas more exposed to the sun, such as the ears, face, 2015) (Fig. 1). Toxicity due to this plant has not been recorded before.
nostrils, teats, udder, vulva, and distal extremities of the limbs. Clini Therefore, the aim of this study was to describe the epidemiological
cally, dermatitis leads to intense itching with subsequent self-inflicted and clinicopathological findings of photosensitization outbreaks in
Fig. 1. Map of Brazil (bottom left) with the geographic distribution of Chamaecrista serpens highlighted in red. The larger map is of the square in the inset and shows
the four microregions in Bahia State, Northeastern Brazil (highlighted in green) where the eleven outbreaks of photosensitization occurred: Queimadas (1), Santaluz
(2), Araci (3), Tucano (4), Pé de Serra (5), Serra Preta (6), Santo Estêvão (7), and Cabaceiras do Paraguaçu (8). (For interpretation of the references to colour in this
figure legend, the reader is referred to the Web version of this article.)
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M.F.F. Mendonça et al. Toxicon 193 (2021) 13–20
Table 1
Serum biochemistry results for the pilot experiment where Ov-0 received Cha
maecrista serpens plant material in the diet for 21 days.
Biochemical parameters D0 D15 D30 Ref. intervalsa
b
GGT (IU/L) 44 – 679 20–52
ASTc (IU/L) 90 349 982 60–280
TBd (mg/dL) 0,2 0,3 1,9 0,1–0,4
DBe (mg/dL) 0,1 0,2 1,1 0-0,27
IBf (mg/dL) 0,05 0,1 0,8 0-0,12
a
Reference intervals by Kaneko et al. (2008).
b
Gamma-glutamyl transferase.
c
Aspartate aminotransferase.
d
Total bilirubin.
e
Fig. 2. Pasture invaded by Chamaecrista serpens in the municipality of Santaluz, Direct bilirubin.
f
Bahia State, Northeastern Brazil. Indirect bilirubin.
15
M.F.F. Mendonça et al. Toxicon 193 (2021) 13–20
further experimentation proceeded (the second experimental study). Thirty days after the beginning of the experiment, the EG animals
Four healthy, crossbred sheep, comprising two adult light brown ewes were removed from the pasture. Ov-1, which had more pronounced skin
(Ov-1 and Ov-2), one five-month-old black ram lamb with a white right lesions, was euthanized and necropsied. During the necropsy, fragments
foot (Ov-3), and one five-month-old white and black spotted ewe lamb of skin from different regions (with and without lesions), organs from
(Ov-4), constituted the experimental group (EG). In order to prove the the abdominal and thoracic cavities, and the brain were collected. The
toxicity of C. serpens in loco, the sheep were introduced into a native Ov-0, Ov-2, Ov-3, Ov-4, Ov-5, and Ov-6 sheep were subjected to skin
pasture where C. serpens was the dominant plant. It appeared highly biopsies. This material was fixed in 10% formalin, processed by routine
palatable for the sheep. This native pasture was on the Santaluz farm histological techniques, stained with hematoxylin-eosin (HE), and
(Fig. 2), where there had been outbreaks of photosensitization in cattle, evaluated under an light microscope.
sheep, and horses 10 years previously. No known photosensitizing After they were removed from the pasture, the EG animals were kept
plants had been found on this property. Two adult light brown ewes (Ov- in shaded paddocks without C. serpens, fed exclusively with Pennisetum
5 and Ov-6), kept on a C. serpens-free pasture on the same farm, served as purpureum and concentrate feed at 1% of live weight and water ad
a control group (CG). The sheep were observed daily for 30 days. All libitum for 45 days, with physical examinations and blood collections
sheep had direct exposure to solar radiation and had water ad libitum. being performed every 15 days (D45, D60, and D75) to assess their
The experiment took place during the end of the rain/winter season, recovery.
between August and September 2019. Rainfall ranged from 12 to 25 mm
during this time (Inmet, 2019). 3. Results
On D0, D15, and D30, the sheep from EG and CG were weighed and
subjected to a comprehensive clinical examination with emphasis on the 3.1. Spontaneous field outbreak
skin. On these occasions, blood samples were collected by puncture of
the jugular vein similar to that performed in the PE. The data provided It was found that, in general, the animals avoided the sun (remaining
by Kaneko et al. (2008) for serum enzyme activities and analyte con in the shade), grazed mainly at night (periods of mild temperature), and
centrations were taken as a reference, as well as the individual values of exhibited hyporexia, weight loss, restlessness, irritability, and severe
each sheep obtained on D0. This way, the EG sheep served as their itching with self-inflicted trauma. The photosensitive skin lesions varied
control, which prevented the occurrence of possible individual in relation to their distribution, size, intensity, and appearance
variations. (Figs. 4–6). Generally, the photodermatitis was progressive and con
All sheep in the PE, EG, and CG were subjected to liver evaluation by sisted of skin hyperemia, edema, ulcerative-crusted lesions with necro
percutaneous liver biopsy guided by ultrasound with catheter no. 14 on sis, especially in non-pigmented skin areas, with loss of epidermis
D0 and repeated on D30. The technique described by Néspoli et al. (extensive dry areas, which were mummified in appearance with cracks
(2010) was adapted. The animals were kept standing, with the catheter and ulcerations). In addition, the lesions in young animals were more
inserted in the 11th intercostal space, after local wool was shaved (10 severe, and there was no sex predilection. In horses, where the outbreak
cm2), surgical antisepsis, and local anesthetic button block with 5 mL of occurred in Santaluz, affecting a mare with a creamy coat, the head was
2% lidocaine hydrochloride (Dorfin®), in the intercostal muscle, with at severely affected by crusty and ulcerative lesions that bleed easily, and
least three liver samples being collected from each animal. the whole body was compromised by scabs (Fig. 6). Other clinical signs
Fig. 4. Cattle naturally intoxicated with Chamaecrista serpens in Bahia State, Northeastern Brazil showing a variety of focal to multifocal photosensitive skin lesions
(A–F). Note itching (C), and bleeding on face due to intense itching (E).
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M.F.F. Mendonça et al. Toxicon 193 (2021) 13–20
Fig. 5. Sheep naturally poisoned by Chamaecrista serpens in Bahia State, Northeastern Brazil showing focally extensive photosensitive skin lesions on the flank and
lateral abdomen (A), and on the back (B).
Fig. 6. Horses naturally poisoned by Chamaecrista serpens in Bahia State, Northeastern Brazil showing photosensitive skin lesions characterized by ulceration and
crusts around the lips, nostrils, muzzle and periorbital regions.
observed in horses were apathy and drowsiness. In the outbreak at Serra hyporexia, irritability, with intense photophobia and moderate to severe
Preta, approximately 50% of the mares showed photosensitive lesions in dermatitis that evolved into scaly ulcerative skin lesions (Fig. 7). The
non-pigmented areas of the body, such as the face and limbs, in addition main clinical signs and outcome observed in sheep experimentally
to body irritation and itching. poisoning by C. serpens are described in Table 2.
Outbreaks of natural poisoning by C. serpens occurred approximately Regarding serum biochemistry, there was a progressive increase in
one week after the animals were introduced to paddocks invaded by the GGT activity in the four sheep of the EG between D0, D15, and D30,
plant at the beginning of the rainy season, when there is great growth of which suggested liver injury caused by the plant. The two control sheep
the plants in the pastures (it is one of the first plants to sprout leaves after showed no variation in GGT levels. Following the removal of the sheep
the first rains). from the pastures on D30, GGT activities steadily decreased on D45 and
The incidence of photosensitization in the spontaneous outbreaks in D60 until recovery on D75 (Fig. 8). There were no notable changes in
cattle and sheep varied between 6% and more than 60%. AST activities or in the concentrations of the other measured analytes.
Ov-1 showed more severe photosensitization, characterized by ul
3.2. Experimental reproduction cerative and necrotizing dermatitis, with hyperemia, alopecia, desqua
mation, and subsequent dermal healing and thickening. These lesions
Pruritus and photophobia were first noticed a few days after sheep in were bilateral and were mainly located on the face, ears, sides of the
the EG began consumption of C. serpens. The clinical signs progressively chest, axillae, flank, pelvis, and back, where they were more extensive
worsened with the animals remaining in the shade, and showing and accentuated. After euthanasia, Ov-1 was necropsied. In addition to
17
M.F.F. Mendonça et al. Toxicon 193 (2021) 13–20
the skin lesions already described, the liver was enlarged, diffusely pale,
and firm, with an evident lobular pattern and an empty gallbladder.
Additionally, there was moderate irregularity in the visceral face of the
left lateral hepatic lobe.
Microscopic evaluation revealed skin and liver changes in the PE and Fig. 9. Photomicrograph of the liver of a sheep experimental poisoned by
EG. In the liver, there was a marked disorganization of the cords of Chamecrista serpens. There is loss of organization of hepatocyte cords, intra
hepatocytes associated with amphophilic intracytoplasmic micro- and cytoplasmic vacuoles, multifocal nuclear pyknosis (arrow), moderate multifocal
macrovacuoles (moderate steatosis), cytoplasmic hypereosinophilia, coagulative necrosis, in addition to the focal area of fibrosis near the periportal
region (PR) (arrowhead) and diffuse increase in eosinophilia. Ov-1. HE. 400x.
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M.F.F. Mendonça et al. Toxicon 193 (2021) 13–20
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M.F.F. Mendonça et al. Toxicon 193 (2021) 13–20
Acknowledgements Leal, P.V., Pupin, R.C., Lima, S.C., Melo, G.K.A., Araújo, M.A., Gomes, D.C., Barros, C.S.
L., Lemos, R.A.A., 2017. Ingestion of the pods of Enterolobium contortisiliquum causes
hepatogenous photosensitization in cattle. Toxicon 131, 6–10. https://doi.org/
Prof. team Luciano Queiroz, botanist responsible for the UEFS Her 10.1016/j.toxicon.2017.03.009.
barium, who registered and cataloged C. serpens. This study was Lorenzi, H., 2008. Plantas daninhas do Brasil - terrestres, aquáticas, parasitas e tóxicas,
financed in part by the Coordenação de Aperfeiçoamento de Pessoal de fourth ed. Inst. Plantarum, Nova Odessa.
Lucena, R.B., Pierezan, F., Kommers, G.D., Irigoyen, L.F., Fighera, R.A., Barros, C.S.L.,
Nível Superior - Brazil (CAPES) - Finance Code 001. 2010. Doenças de bovinos no Sul do Brasil: 6.706 casos. Pesqui. Vet. Bras. 30 (5),
428–434. https://doi.org/10.1590/S0100-736X2010000500010.
References Méndez, M.C., Riet-Correa, F., Schild, A.L., Ferreira, J.L., Pimentel, M.A., 1991.
Fotossensibilização em bovinos causada por Ammi Majus. Pesqui. Vet. Bras. 11 (1),
17–19.
Albernaz, T.T., Silveira, J.A.S., Silva, N.S., Oliveira, C.H.S., Reis, A.S.B., Oliveira, C.M.C., Mendonça, F.S., Evêncio-Neto, J., Baratella-Evêncio, L., Dória, R.G.S., Freitas, S.H.,
Duarte, M.D., Barbosa, J.D., 2010. Fotossensibilização em ovinos associada à Pelegrini, L.F., Cruz, R.A.S., Ferreira, E.V., Colodel, E.M., 2009. Natural and
ingestão de Brachiaria brizantha no estado do Pará. Pesqui. Vet. Bras. 30 (9), experimental poisoning of cattle by Enterolobium contortisiliquum pods (Fabaceae
741–748. https://doi.org/10.1590/S0100-736X2010000900006. Mimosoideae) in Central-Western Brazil. Acta Vet. 78 (4), 621–625. https://doi.org/
Araújo, V.O., Oliveira Neto, T.S., Simões, S.V.D., Silva, T.K.F., Riet-Correa, F., Lucena, R. 10.2754/avb200978040621.
B., 2017. Primary photosensitization and contact dermatitis caused by Malachra Néspoli, P.B., Gheller, V.A., Peixoto, P.V., França, T.N., Carvalho, A.U., Araújo, D.K.G.,
fasciata Jacq. N.V. (Malvaceae) in sheep. Toxicon 138, 184–187. https://doi.org/ Malm, C., 2010. Avaliação de técnicas de biópsia hepática em ovinos. Pesqui. Vet.
10.1016/j.toxicon.2017.09.009. Bras. 30 (1), 29–36.
Brum, K.B., Haraguchi, M., Garutti, M.B., Nóbrega, F.N., Rosa, B., Fioravanti, M.C.S., Neto, M.J., 2010. Levantamento florístico e colonização micorrízica em dois
2009. Steroidal saponin concentrations in Brachiaria decumbens and B. brizantha at remanescentes de cerrado típico e em plantas ruderais no município de Três Lagoas-
different developmental stages. Ciência Rural. 39 (1), 279–281. https://doi.org/ MS (Aleph).
10.1590/S0103-84782008005000034. Olinda, R.G., Medeiros, R.M.T., Dantas, A.F.M., Lemos, R.A.A., Riet-Correa, F., 2015.
Collett, M.G., 2019. Photosensitisation diseases of animals: classification and a weight of Intoxicação por Enterolobium contortisiliquum em bovinos na região Nordeste do
evidence approach to primary causes. Toxicon X 3, 100012. https://doi.org/ Brasil. Pesqui. Vet. Bras. 35 (1), 44–48. https://doi.org/10.1590/S0100-
10.1016/j.toxcx.2019.100012. 736X2015000100010.
Constable, P.D., Hinchcliff, K.W., Done, S.H., Grunberg, W., 2017. Diseases of skin, eye, Paula, E.F.E., Stupak, E.C., Zanatta, C.P., Poncheki, J.K., Leal, P.C., Monteiro, A.L.G.,
conjunctiva and external ear. In: Constable, P.D., Hinchcliff, K.W., Done, S.H., 2009. Comportamento ingestivo de ovinos em pastagem: uma revisão. Rev. Trópica
Grunberg, W. (Eds.), Veterinary Medicine - A Textbook of the Diseases of Cattle, Ciencias. Agrar. e Biol. 4 (1), 42–51.
Sheep, Goats, Pigs, and Horses, eleventh ed. Elsevier Health Sciences, St. Louis, Pimentel, L.A., Riet-Correa, F., Guedes, K.M.R., Macêdo, J.T.S.A., Medeiros, R.M.T.,
pp. 1549–1551. Dantas, A.F.M., 2007. Fotossensibilização primária em equídeos e ruminantes no
Dal-Pizzol, J.G., Biasiolo, R., Raupp, G.T., Baldissera, J.N.C., Almeida, E.X., Ribeiro semi-árido causada por Froelichia humboldtiana (Amaranthaceae). Pesqui. Vet. Bras.
Filho, H.M.N., 2019. Consumo de forragem por ovinos ingerindo grama missioneira 27 (1), 23–28. https://doi.org/10.1590/S0100-736X2007000100005.
gigante com ou sem acesso a amendoim forrageiro. Arq. Bras. Med. Vet. Zootec. 71 Pupin, R.C., Melo, G.K.A., Heckler, R.F., Faccin, T.C., Ítavo, C.C.B.F., Fernandes, C.E.,
(2), 623–630. https://doi.org/10.1590/1678-4162-10404. Gomes, D.C., Lemos, R.A.A., 2016. Identification of lamb flocks susceptible and
Faccin, T.C., Riet-Correa, F., Rodrigues, F.S., Santos, A.C., Melo, G.K.A., Silva, J.A., resistant against Brachiaria poisoning. Pesqui. Vet. Bras. 36 (5), 383–388. https://
Ferreira, R., Ítavo, C.C.B.F., Lemos, R.A.A., 2014. Poisoning by Brachiaria brizantha doi.org/10.1590/S0100-736X2016000500005.
in flocks of naïve and experienced sheep. Toxicon 82, 1–8. https://doi.org/10.1016/ Resende, K.T., Silva, H.G.O., Lima, L.D., Teixeira, I.A.M.A., 2008. Avaliação das
j.toxicon.2014.02.008. exigências nutricionais de pequenos ruminantes pelos sistemas de alimentação
Ferreira, E.V., Boabaid, F.M., Arruda, L.P., Lemos, R.A.A., Souza, M.A., Nakazato, L., recentemente publicados. Rev. Bras. Zootec. 37, 161–177.
Colodel, E.M., 2009. Intoxicação por Stryphnodendron fissuratum (Mimosoideae) em Riet-Correa, F., Haraguchi, M., Dantas, A.F.M., Burakovas, R.G., Yokosuka, A.,
bovinos. Pesqui. Vet. Bras. 29 (11), 951–957. https://doi.org/10.1590/s0100- Mimaki, Y., Medeiros, R.M.T., Matos, P.F., 2009. Sheep poisoning by Panicum
736x2009001100015. dichotomiflorum in northeastern Brazil. Pesqui. Vet. Bras. 29 (1), 94–98. https://doi.
Grecco, F., Dantas, A.F.M., Riet-Correa, F., Leite, C.D., Bonel-Raposo, R., 2002. Cattle org/10.1590/s0100-736x2009000100015.
intoxication from Enterolobium contortisiliquum pods. Vet. Hum. Toxicol. 44 (3), Rissi, D.R., Rech, R.R., Pierezan, F., Gabriel, A.L., Trost, M.E., Brum, J.S., Kommers, G.D.,
160–162. Barros, C.S.L., 2007. Intoxicações por plantas e micotoxinas associadas a plantas em
Hargis, A.M., Myers, S., 2017. The integument. In: Zachary, J.F. (Ed.), Pathologic Basis of bovinos no Rio Grande do Sul: 461 casos. Pesq. Vet. Bras 27 (7), 261–268. https://
Veterinary Disease, sixth ed. Elsevier, St. Louis, pp. 1009–1146. doi.org/10.1590/s0100-736x2007000700002.
Hoffmann, W.E., Solter, P.F., 2008. Diagnostic enzymology of domestic animals. In: Rowe, L.D., 1989. Photosensitization problems in livestock. Vet. Clin. North Am. Food
Kaneko, J.J., Harvey, J.W., Bruss, M.L. (Eds.), Clinical Biochemistry of Domestic Anim. Pract. 5 (2), 301–323. https://doi.org/10.1016/S0749-0720(15)30978-6.
Animals, sixth ed. Academic Press, San Diego, pp. 351–378. https://doi.org/ Silva Filho, G.B., Chaves, H.A.S., Albuquerque, R.F., Souza, P.E., Vieira, M.E.Q.,
10.1016/B978-0-12-370491-7.00012-X. Nascimento, A.L.O., Lima, S.C., Mendonça, F.S., 2020. Spontaneous and
Inmet, 2019. Relatórios de precipitações pluviométricas no Brasil accessed. http://www. experimental poisoning by Froelichia humboldtiana in cattle. Pesqui. Vet. Bras. 40 (1),
clima.inmet.gov.br/prec/. (Accessed 29 July 2020). 1–6. https://doi.org/10.1590/1678-5150-PVB-6351.
Kaneko, J.J., Harvey, J.W., Bruss, M.L., 2008. Clinical Biochemestry of Domestic Souza, R.I.C., Riet-Correa, F., Brum, K.B., Fernandes, C.E., Barbosa-Ferreira, M.,
Animals, sixth ed. Academic Press, San Diego. Lemos, R.A.A., 2010. Intoxicação por Brachiaria spp. em bovinos no Mato Grosso do
Knupp, S.N.R., Borburema, C.C., Oliveira Neto, T.S., Medeiros, R., Knupp, L.S., Riet- Sul. Pesqui. Vet. Bras. 30 (12), 1036–1042. https://doi.org/10.1590/s0100-
Correa, F., Lucena, R.B., 2014. Surtos de fotossensibilização primária em equídeos 736x2010001200006.
causados por Froelichia humboldtiana. Pesqui. Vet. Bras. 34 (12), 1191–1195. Souza, V.C., Bortoluzzi, R.L.C., 2015. Chamaecrista in Lista de Espécies da Flora do Brasil.
Lazaro, N.D., Bacha, F.B., Pupin, R.C., Paula, J.P.L., Leal, P.V., Pott, A., Gomes, D.C., Jardim Botânico do Rio de Janeiro accessed. http://floradobrasil.jbrj.gov.br/jabot
Lemos, R.A.A., 2018. Photosensitization in cattle caused by spontaneous and /floradobrasil/FB28071/. (Accessed 20 July 2020).
experimentally ingestion of Stryphnodendron fissuratum. Acta Sci. Vet. 46, 1–8. Tokarnia, C.H., Brito, M.F., Barbosa, J.D., Peixoto, P.V., Dobereiner, J., 2012. Plantas
https://doi.org/10.22456/1679-9216.81829. Tóxicas do Brasil para Animais de Produção, second ed. Helianthus, Rio de Janeiro.
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