Pesq. Vet. Bras. 37(7):662-666, julho 2017

Sudden death associated with Niedenzuella stannea () in cattle in the State of Mato Grosso, Brazil: importance and epidemiological aspects1

Flávio H.B. Caldeira2, Geovanny B.G. Dias2, 2, Valdecy de M. Lourenço3, Kalinne S. Bezerra2 4 and Edson Moleta Colodel5* Felipe P. de Arruda ABSTRACT.- , Franklin Riet-Correa F. & Colodel E.M. 2017. Sudden death associated with Niedenzuella stannea (Malpighi- aceae) in cattleCaldeira in the F.H.B., State Dias of MatoG.B.G., Grosso, Arruda F.P.,Brazil: Lourenço importance V.M., Bezerra and epidemiological K.S., Riet-Correa aspects. Pesquisa Veterinária Brasileira 37(7):662-666. Departamento de Clínica Médica -

BoaVeterinária, Esperança, Faculdade Cuiabá, deMT Agronomia, 78069-900, Medicina Brazil. E-mail: Veterinária [email protected] e Zootecnia, Universidade Fe deralThe de aim Mato of Grosso,this study Campus was to Universitário, investigate the Av. importance Fernando Corrêa of an acuteda Costa disease 2367, that Bairro was characterized by sudden death associated with exercise that affected cattle in the region of

- edthe and Araguaia the pastures River, especially of these farmsin the weremunicipality inspected. of Torixoréu,Epidemiological southeastern questionnaires Mato Grosso, were Brazil. Between August and September 2013, eightyNiedenzuella farms in thestannea municipality (N. stannea) were of visit the Malpighiaceae family was attributed to the cause of sudden death in cattle, what causes majorcompleted economic from 65losses. farms. Sudden A death identified reports as have occurred since 1970, when livestock was introduced into the region, and sudden death reports still occur. Outbreaks were re- ported to occur from May to October, but mainly during the dry season between June and N. stannea

manualAugust. application was of Tordon identified® (Picloram at 41 farms and 2.4D).and was The always administration found in near of 5g/kg to rivers. of young The leavesmost effective which were plant collected control methods from a farm included with aplowing sudden the death pastures history and in cattlefields followedalso caused by sudden death in a sheep. Thus, it is concluded that the sudden death of cattle in the region N. stannea. Niedenzuella stannea, Malpighiaceae, plant poisoning, suddenof the Araguaia death, cattle, River experimental is caused bypoisoning, the consumption sheep, Mato of Grosso. INDEX TERMS: Poisonous , toxic plants, 1 RESUMO.- [Morte súbita associada a Niedenzuella stan- nea (Malpighiaceae) em bovinos no Estado de Mato 2 Received on September 7, 2016. Grosso: importância e investigação epidemiológica.] O Accepted for publication on August 2, 2017. - objetivo deste trabalho é relatar a investigação sobre uma Programa de Pós-Graduação em Ciências Veterinárias, Faculdade de enfermidade de caráter agudo, caracterizada por morte sú- BoaAgronomia, Esperança, Medicina Cuiabá, Veterinária MT 78068-900, e Zootecnia Brazil. (Famevz), Universidade Fe deral3 de Mato Grosso (UFMT), Av. Fernando Corrêa da Costa 2367, Bairro bita associada ao exercício, que acomete bovinos na região

4 Instituto de Defesa Agropecuária do Estado de Mato Grosso (Indea/ município de Torixoréu, sudeste do estado de Mato Grosso, MT), Rua Bela Vista s/n, Centro, Torixoreu, MT 78260-000, Brazil. - Brasil.de bacias Entre hidrográficas agosto e setembro do Rio Araguaia, de 2013, especialmenteforam visitadas no e de, Patos,Laboratório PB 58700-310, de Anatomia Brazil. Patológica, Hospital Veterinário, Centro de inspecionadas as pastagens em 80 propriedades rurais do Saúde5 e Tecnologia Rural (CSTR), Universidade Federal de Campina Gran Departamento de Clínica Médica Veterinária (Climev), Faculdade de município, e em 65 aplicado um questionário epidemioló- - Niedenzuella stannea daAgronomia, Costa 2367, Medicina Bairro BoaVeterinária Esperança, e Zootecnia Cuiabá, MT(Famevz), 78069-900, Universidade Brazil. *Cor Fe- (Malpighiaceae), é incriminada como causadora de morte respondingderal de Mato author: Grosso [email protected] (UFMT), Campus Universitário, Av. Fernando Corrêa súbitagico. Uma em bovinos planta identificadagerando grandes como prejuízos econômicos.

662 Sudden death associated with Niedenzuella stannea (Malpighiaceae) in cattle in the State of Mato Grosso, Brazil 663

- - ária começou a ser inserida na região, e ocorrem até os dias atuais.Relatos Surtos de morte ocorreram súbita datam em diferentes desde 1970, meses quando do ano, a pecu va- municipalityden death history; of Torixoréu these cattle (16o11’58”S, farms were 52o33’20”W), identified Mato by the Grosso Offi riando de maio a outubro, sendo a maior parte concentrada ce of Agricultural Protection of Mato Grosso (Indea/MT) in the- durante o período de seca, especialmente nos meses de ju- (MT), midwestern Brazil. The farms were located in the Araguaia- nho a agosto. N. stannea - ries-Tocantins of Diamantino, River Basin Guariroba on the banksand Quebra-Dente of the Araguaia Creeks. River GPS and Tra its- des, sendo presente próxima aos leitos de rios. Os métodos ckMakertributaries software, including version the Diamantino 13.8.517 was River used and to the obtain main thetributa geo- foi identificada em 41 proprieda graphical coordinates of the farms after the properties bordering o arar da pastagem e roça manual seguida da aplicação de these rivers were selected using Google EarthTM, version 7.0.8415. Tordonde controle® da planta relatados como mais eficazes foram The properties were systematically visited to distribute the epi- de 5g/kg de folhas em brotação de N. stannea, coletadas em demiological questionnaire, to inspect the pastures and mark the uma propriedade (Picloram com e 2,4D). histórico A administração de morte súbita para um em ovino, bovi- location using a global positioning system (GPS). nos, reproduziu o quadro de morte súbita. Conclui-se que The epidemiological survey was given to the owners and em- as mortes súbitas em bovinos em áreas da bacia hidrográ- ployees of the farms to collect data regarding the characteristics of - N. stannea. Niedenzuella stannea, Photosthe farms, published outbreaks by Tokarniaof sudden et death al. (2012) and mortality of the main control. plants A thatmo Malpighiaceae,fica do rio Araguaia intoxicação se devem por plantas, ao consumo morte súbita, de bovinos, in- causedified suddenmodel of death forms in 2 Brazil and 3 wereused shownby Silva to et the al. (2006)interviewed was used. sub- toxicaçãoTERMOS DEexperimental, INDEXAÇÃO: ovino, Plantas Mato tóxicas, Grosso. jects for possible recognition of these plants in the region. Collection of plant samples. Samples were collected of only INTRODUCTION the that were suggested by the interviewed subjects as causing the disease and that were found on farms where the occur- Sudden death is important in livestock in Brazil because it is responsible for at least half of the cattle deaths caused by samples collected in November 2012 from a farm that was visited the consumption of plants in the country (Tokarnia et al. (16°18’41.38”S,rence of sudden 52°56’01.77”W)death in cattle was were frequent. sent to Leaf, the University fruit and flower of Mi- 2012). The major plants associated with this type of poiso- Experimental poisoning. Sprouting leaf samples of a similar Malpighiaceae (Tokarnia et al. 2012). In the Malpighiaceae chigan Ervaarium (Michigan, USA) for botanical identification. family,ning belong Amorimia to three septentrionalis families: Rubiaceae, and A. rigida Bignoniaceae stand out and as to a male sheep at a dose of 5g/kg body weight (bw). Six hours the most important toxic plants in the Northeast (Tokarnia plant that were sent for identification were orally administered- et al. 1990, 2012, Duarte et al. 2013), whereas A. exotropi- ter the exercise, a clinical examination was performed including monitoringafter administration of respiratory of the plant, movements, the sheep behavior, was forced posture to run. and Af ca is the most important toxic plant in the South (Gava et al. 1998, Pavarini et al. 2011) and A. sepium in the North recorded, and samples of the liver, kidney, heart, lung, intestine, (Schons et al. 2011); however, considering the geographic lymphconsumption nodes, ofspleen water and and brain food. were At necropsy, collected. gross The samples lesions were - Lee et al. 2012 suggested that the species is probably A. - Amazonicalocation of .the Poisonings outbreaks by in A. Brazil pubiflora and photoin the identification, Midwest and malfixed research in 10% formalin,was approved routinely by the processed Ethical forCommittee histology, in and the stai Use Southeast have also been reported (Tokarnia & Döbereiner ned with hematoxylin and eosin for histologic evaluation. All ani 1973, Becker et al. 2013). Numerous plant species that cause sudden death in li- of Experimental Animals of the Federal University of Mato Grosso - (CEUA-UFMT) (protocol 23108016273/13-0).RESULTS Botanical identification vestock contain the toxic organofluorine compound mono The plant that was suspected to cause sudden death in thatfluoroacetate are dependent (MFA) on (Lee energy et al. (Clarke2012), which1991). decreases In cattle, the the rural area of the municipality of Torixoréu was identi- primaryproduction effects of ATP occur and in blocksthe heart other and metabolic cause sudden processes dea- Niedenzuella stannea - derson, which belongs to the Malpighiacea family. and death are precipitated by exercise (Lemos et al. 2011, fied as the species (Griseb.) W.R. An Tokarniath (Maxie et & al. Robinson 2012, Becker 2007). et al.In 2013);most cases, but the clinical occurrence signs Epidemiologic study of poisoning depends on many factors such as palatability, Eighty farms in the municipality of Torixoréu were vi- sited, and all the pastures were inspected. Of these farms, variations (Pessoa et al. 2013). people were available to answer the epidemiological ques- hunger,The aimsprouting of this after study the was first to rains,investigate and dose the andimportance toxicity of an acute disease characterized by sudden death associa- ted with exercise, which affects cattle in the region of the tionnaire on 65 farms. Of the respondents, 40 (61.53%)- vices.were owners,From the 17 65 (26.15%) properties were where cowherds, interviews five were (7.69%) per- the southeastern region of the State of Mato Grosso, Brazil. were managers, and three (4.61%) performed general ser Araguaia River, especially in the municipality of Torixoréu in among cattle. The oldest reports date back to 1970 when MATERIALS AND METHODS livestockformed, 33 activity (50.76%) began reported in the region, a history and ofcurrently sudden deaths death Epidemiologic study. are still reported. The main clinical signs reported by the conducted by selecting cattle farms located in regions with a sud- respondents had a common relationship with the move- A descriptive observational study was

Pesq. Vet. Bras. 37(7):662-666, julho 2017 664 Flávio H.B. Caldeira et al. ment of cattle, in which parties described the following cli- nical signs: rough hair coat, frequent urination, trembling, often associated the death of the animal with the arrival at theweakness, barn (described drooling, asfalling barn and odor). dying quickly. Respondents The outbreaks occurred in different months of the year, ranging from May to October and mainly during the dry that when the dry period of the year starts, the pastures andseason other between invasive June plants and begin August. to “dry”, Respondents and Niedenzuella reported stannea begins to sprout in this period. This plant was des- cribed to be more visible or even the only “green” plant in the pasture. During this time, the cattle begin to consume the plant, and mortality begins. N. stannea was attributed Fig.1. Independence Farm, Torixoréu, Mato Grosso, Brazil. (A) by all respondents to be responsible for causes of sudden Green Niedenzuella stannea in a pasture of dry Brachiaria spp. death in cattle. Of the 33 farms with a history of sudden de- (B) Cattle consuming leaves of N. stannea C) ath, all respondents reported the occurrence of N. stannea. Sprouts of N. stannea. (D) Flowers and fruits of N. stannea. in August 2013. ( In seven of these properties, the plant has been eradica- of the inspection was to identify known toxic plants that the plants presented in the photos, including plants in the cause sudden death and the presence of the plant that res- ted, and recognition was confirmed by the photos. None of death in cattle, were recognized by respondents or found on 41 properties in the region (Fig.1) and it was exclu- duringRubiaceae a survey or Bignoniaceae of the pasture family areas known or surrounding to cause suddenforests. sivelypondents present termed on “Erva”.properties This that “Erva” border plant the was main identified rivers Forms of disease control were reported in all of the pro- of the municipality, namely, the Guariroba, Quebra-Dente, perties and included plant control and control of the ma- observed to infest areas next to the banks of rivers and most effective management method, which eradicated the closeDiamantino to riparian and forests, Araguaia and Rivers it was (Fig.2). also found The in plant areas was of plant,nifestation was to of plow the intoxication. the pastures Regarding infested with plant N. stanneacontrol, (onthe dense forest but in areas no more than 500 meters from two properties) or cutting followed by the application of the riverbanks. The respondents described that the plant Tordon® - can only be developed where the land is more favorable pondents claimed that manual weeding increased the oc- for agriculture. This visit occurred during the month of currence (Picloramof poisonings + 2.4D) due to(on regrowth five properties). of the plant, Some which res is more attractive to cattle. On properties where the plant the species incriminated by respondents as responsible was not controlled, some owners prevented animal access forAugust, causing and sudden there was death abundant in cattle. flowering No case of and spontaneous fruiting of to the plants by surrounding these areas (i.e., fencing). Ow- poisoning was observed during the visits. Palicourea mar- ners often reported that when they needed to use the area cgravii, Amorimia pubiflora or other plant species known with N. stannea present, they put the calves (weanlings) in to cause sudden death in livestock were not observed du- these areas because the mortality of young animals would ring these surveys and were not mentioned during the cause less economic damage. questioning. The control of the manifestation of intoxication was Experimental poisoning mostly occurred after the movement of cattle, constant For the experimental poisoning, six hours after the ad- handlingfocused onwas management avoided, except practices. for obligatory As the clinicalvaccinations. signs ministration of 5g/kg bw of leaves, the sheep was forced to However, this management method creates access to pas- run for two minutes, and the following clinical signs were tures that contain N. stannea during free pasture; the cattle noted: muscle spasm, paddling movements, tachycardia, arrive in the free pastures and remain there for a period of engorgement of the jugular, positive venous pulse, opistho- performed. - tonos and nystagmus. The sheep died within five minutes fiveThe to 15 mortality days. After related this to time, the managementconsumption practicesof N. stannea are ffusely congested lung and the presence of foam in the tra- reported by the respondents showed variation with rates chea.after theEngorgement fall. A necropsy of the was cranial performed vena cava and andrevealed petechiae a di - - mals recovered, but there were no precise rates of morbi- croscopic changes were observed. dity.of 0.2% This to research 8% of the reported herd each that year. at least In addition, 573 cattle some and anione in the pericardium were also observed. No significant mi buffalo died based on the presentation of sudden death in DISCUSSION AND CONCLUSIONS the last 43 years and on the different properties. In Brazil, Niedenzuella stannea Pantanal regions and has a geographical distribution in the Inspection of pastures states of Pará, Mato Grosso and isMato found Grosso in the do Amazon Sul (Mame and- Inspection of the pastures was performed on 80 far- de 2014). The Niedenzuella ms in the municipality of Torixoréu, Mato Grosso. The aim the genus and Tetrapterys, presents morpholo- , previously classified in

Pesq. Vet. Bras. 37(7):662-666, julho 2017 Sudden death associated with Niedenzuella stannea (Malpighiaceae) in cattle in the State of Mato Grosso, Brazil 665

Nieden- zuella stannea up to 307m from the river bank. Fig.2. Bacuri Farm, Torixoréu, Mato Grosso. The demarcated area near the Quebra-Dente River (circled in red) was infested by gical characteristics similar to the other species of Malpi- N. stannea - ted with plant consumption are infrequent. Barbosa et al. species are known to be toxic to cattle, there are no pre- (2003) reported. Reports that of this sudden species death is upin tobuffaloes six times associa more viousghiaceae reports (Anderson in the 2006).literature Although indicating many poisoning Malpighiaceae by N. resistant to poisoning by Palicourea marcgravii. stannea. The infestation by N. stannea in the pastures was This epidemiological survey showed that the plant po- found close to the riverbanks including riparian forests. Niedenzuella This plant was also found in distant and dense forest are- stannea, is the cause of sudden death in cattle in the muni- as, but it was limited to a distance of less than 500 meters cipalitypularly calledof Torixoréu, “Erva”, whichMT. Evidence was identified showed as that mortality was present only in pastures where N. stannea was found. grows only where the land is more favorable for agricultu- re.from These the riverbanks. features have Respondents also been described reported thatin other the plant Mal- sudden death cases ceased when the plant was eradicated. pighiaceae, such as Amorimia pubiflora, which inhabits Reductions of mortality occurred with plant control, and fertile soils, and A. rigida and A. Amazonica, which grow with the administration of N. stannea to a sheep. In addi- in areas close to rivers (Schons et al. 2011, Tokarnia et al. tionAdditionally, to these infactors, this study, other suddenplants thatdeath cause was sudden reproduced dea- 2012). th, such as Palicourea marcgravii (Tokarnia & Döbereiner pubiflora (Becker et of Malpighiaceae such as A. pubiflora (Becker et al. 2013), A. rigidaDifficulty and inA. septentrionalis controlling and is eradicating a common characteristic some species Brazil,1986) andwere Albuquerque not found during et al. the 2014, inspection of the pastu- of these plants al. 2013), which cause poisoning in the Midwest Region of 2014), which may be related to the fact that they have a recognized Palicourea marcgravii, but Amorimia spp. was deep root system(Tokarnia that facilitates et al. 2012,regrowth. Albuquerque The economic et al. res. Using photo identification, none of the respondents impact of the control of this disease related to the con- sumption of N. stannea cannot be calculated as there is no 2006).often identified as “Erva”, which may have been due to the accurate information on the cost to reform pastures, of la- morphologicalPoisoning by similarity N. stannea between was most the often plants related (Anderson to bo- bor and the purchase of pesticides. Generally, the owners vine species. The most visited properties had horses that grazed in common areas more than cattle, but there was no most effective poisoning control measures reported by res- record of sudden death or other evidence indicating into- pondentscomplained were about soil the plowing high costs and of manual this control. cutting Among followed the xication in horses. One property reported an occurrence of by application of a product that contains picloram 2.4 D., sudden death in a buffalo that grazed in the pastures with but the economic costs of this method can inhibit its prac-

Pesq. Vet. Bras. 37(7):662-666, julho 2017 666 Flávio H.B. Caldeira et al. tice, especially in large areas and in areas with high infesta- tion. The report indicates that the majority of owners used, Clarke D.D. 1991. Fluoroacetate and fluorocitrate: mechanism of action. Amori- due to costs, techniques that control the manifestation of Neurochem. Res. 16(9):1055-1058. mia clinical poisoning such as proper handling of the animals Duarte A.L., Medeiros R.M.T. & Riet-Correa F. 2013. Intoxicação por and resting in an area free of N. stannea. Some people re- spp. em ruminantes. Ciência Rural 43(7):1294-1301. Mortes súbitas em bovinos causadas pela ingestão de Mascagnia sp. (Mal- ported that they prefer to let younger cattle graze in pastu- Gavapiguiaceae) A., Cristani no J., Estado Branco de J.V., Santa Neves Catarina. D.S., Mondadori Pesq. Vet. A.J.Bras. & Souza18(1):16-20. R.S. 1998. res infested by the plant because it reduces the economic impact of mortality. Manual cutting that is used to control MT.

> Accessed August 2015. the Theinfestation death of has 573 proven cattle inefficient was used todue calculate to the occurrence the direct Palicourea and costsof more of mortalityintensified by regrowth. Niedenzuella stannea poisoning. Con- LeeAmorimia S.T., Cook species. D., Riet-Correa Toxicon 60:791-796. F., Pfister J.A., Anderson W.R., Lima F.G. & sidering an average body weight of 300 kg at US$ 2.40 per Gardner D.R. 2012. Detection of monofluoroacetato in

Lemos R.A.A., Guimarães E.B., Carvalho N.M., Nogueira A.P.A., Santos B.S.,- by poisoning on these farms where interviews occurred Souza R.I.C., Cardinal S.G. & Kassab H.O. 2011. Plant poisonings in Mato wouldkg (IMEA equate 2015), to US$ the 206.280cost attributed. However, to thethis deathnumber of iscattle cle- International,Grosso do Sul, Wallingford,p.68-72. In: Riet-Correa UK. F., Pfister J., Schild A.L. & Wieren ga T. (Eds), Poisoning by Plants, Mycotoxins, and Related Toxins. CAB arly underestimated as this information was obtained from Mamede M.C.H. 2014. Niedenzuella in: Lista de Espécies da Flora do Brasil. people currently on the farm during the interview and ex- - cluded data from previous owners or employees. For a bet- radobrasil/FB101449 ter understanding of poisoning by N. stannea, experimental Jardim Botânico do Rio de Janeiro. Accessed May 2014. studies must be conducted to analyze the clinical and pa- Maxie M.G. (Ed.), Jubb, Kennedy, and Palmer’s Pathology of Domestic thological effects and the technical and economic viability Maxie M.G. & Robinson W.S.F. 2007. Cardiovascular system,737p. p.1-105. In. of control methods for this plant. Pavarini S.P., Soares M.P., Bandarra P.M., Gomes D.C., Bandinelli M.B., Cruz C.E.F.Animals. & Driemeier Vol.3. 5th ed.D. 2011.Saunders Mortes Elsevier, súbitas Philadelphia. em bovinos causadas por Amorimia exotropica Acknowledgements.- Bras. 31:291-296 - (Malpighiaceae) no Rio Grande do Sul. Pesq. Vet. The authors are grateful toDr. William R.Anderson, - 156883/2014)University of Michigan and the Herbarium,National Institute Ann Arbor, of Science Michigan, and Technology USA, for bota for mica, epidemiologia e controle das intoxicações por plantas no Brasil. nic identification and to Mato Grosso State Research (FAPEMAT-Proc. PessoaPesq. C.R.M.,Vet. Bras. Medeiros 33(6):752-758 R.M.T. & Riet-Correa F. 2013. Importância econô Amo- the Control ofPlantpoisonings(INCT/CNPq) for financial support. REFERENCES rimia (Mascagnia) septiumin sheep in northern Brazil. Toxicon 57:781- Schons786. S.V., Mello T.L., Riet-Correa F. & Schild AL. 2011. Poisoning by - ciada à intoxicação por Amorimia septentrionalis em bovinos. Pesq. Vet. AlbuquerqueBras. 34(5):433-437. S.S.C., Rocha B.P. & Almeida V.M. 2014. Fibrose cardíaca asso SilvadoNorte. D.M., Riet-CorreaPesq. Vet. Bras. F., Medeiros26:223-236. R.M.T. & Oliveira O.F. 2006. Plantas Mascag- tóxicas para ruminantes no Seridó Ocidental e Oriental do Rio Grande nia (Malpighiaceae). Novon 16:168-204. Tokarnia C.H. & Döbereiner J. 1973. Intoxicação por Mascagnia pubiflora Anderson W.R. 2006. Eight segregates from the neotropical genus - Tokarnia C.H. & Döbereiner J. 1986. Intoxicação por Palicourea marcgravii ração da sensibilidade de bovinos e búfalos à intoxicação por Palicourea em bovinos no Estado do Mato Grosso. Pesq. Agropec. Bras. 8:61-68. Barbosamarcgravii J.D., Oliveira C.M.C., Tokarnia C.H. & Riet-Correa F. 2003. Compa Tokarnia C.H., Peixoto P.V. & Döbereiner J. 1990. Poisonous plants affecting (Rubiaceae) em bovinos no Brasil. Pesq. Vet. Bras. 6:73-92. Correa­ F., Lee (Rubiaceae). S.T. & Colodel Pesq. E.M. Vet. 2013. Bras. Importância23(4):167-172. da intoxicação por heart function of cattle in Brazil. Pesq. Vet. Bras. 10:1-10. BeckerAmorimia M., Caldeira pubiflora F.H.B., (Malpighiaceae) Carneiro F.M., em Oliveira bovinos L.P., em Tokarnia Mato Grosso: C.H., Riet- re- Tokarnia C.H., Brito M.F., Barbosa J.D., Peixoto P.V. & Döbereiner J. 2012. produção experimental da intoxicação em ovinos e bovinos. Pesq. Vet. - Bras. 33(9):1049-1056. Plantas Tóxicas do Brasil para Animais de Produção. 2ª ed. Editora He lianthus, Rio de Janeiro.

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