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Protodioscin levels in Brachiaria spp. in a sheep production system and a brief review of the literature of Brachiaria spp. poisoning in ruminants

Níveis de protodioscina em Brachiaria spp. em um sistema de produção de ovinos e uma breve revisão da literatura da intoxicação por Brachiaria spp. em ruminantes

ABSTRACT:

Plants of the genus Brachiaria, used in several countries as forage, are poisonous to some livestock species. Their toxic principle is protodioscin, and the main form of clinical presentation of the toxicosis is hepatogenous photosensitization. Here we compare protodioscin levels in B. decumbens and B. brizantha and review the literature on the concentrations and methodologies of collection and analysis of the toxic principle in Brachiaria spp. and the risk of contamination of pastures by more toxic species that may facilitate poisoning by plants of this genus in sheep. The experiment was conducted in pastures originally formed by B. brizantha, with many B. decumbens invasion points. The occurrence of cases of poisoning by Brachiaria spp. was the criterion for confirming pasture toxicity. The forage samples were collected at ten random points every 28 days through manual grazing simulation. The samples were analyzed for protodioscin by high-performance liquid chromatography (HPLC) with light scattering by evaporation (ELSD) after being dried and crushed. In the flock of 69 sheep, five poisoning cases occurred, three sheep died, and two recovered. The protodioscin levels found in the evaluated pastures ranged from 0.70 to 0.45%; higher levels appeared in B. decumbens (7.09%) compared to 1.04% in B. brizantha. We suggest that Brachiaria spp. should be avoided in pastures where sheep are grazing.

INDEX TERMS:
Protodioscin levels; Brachiaria spp.; sheep; ovine; toxic plants; plant poisoning; ruminants; hepatogenic photosensitization; photodermatitis; tropical pasture; ruminant; steroidal saponins

RESUMO:

Plantas do gênero Brachiaria, utilizadas em vários países como forragem, são tóxicas para várias espécies pecuárias. Seu princípio tóxico é a protodioscina, e a principal forma de apresentação clínica da toxicose é a fotossensibilização hepatógena. Este estudo teve como objetivo comparar os níveis de protodioscina em B. decumbens e B. brizantha e revisar a literatura sobre as concentrações e metodologias de coleta e análise do princípio tóxico em Brachiaria spp. e o risco de contaminação das pastagens por espécies mais tóxicas que podem facilitar a intoxicação por plantas desse gênero em ovinos. O experimento foi conduzido em pastagens originalmente formadas por B. brizantha, com diversos pontos de invasão por B. decumbens. Ocorrência de casos de intoxicação por Brachiaria spp. foi o critério para confirmação da toxicidade da pastagem. As amostras de forragem foram coletadas a cada 28 dias em dez pontos aleatórios por meio de simulação de pastejo manual. As amostras foram analisadas para protodioscina por cromatografia líquida de alta eficiência (HPLC) com dispersão de luz por evaporação (ELSD) após serem secadas e trituradas. No rebanho de 69 ovelhas, cinco desenvolveram a intoxicação, três morreram e duas se recuperaram. Os níveis de protodioscina encontrados nas pastagens avaliadas variaram de 0,70 a 0,45%; níveis mais elevados apareceram em B. decumbens (7,09%) em comparação com 1,04% em B. brizantha. Sugerimos que Brachiaria spp. deve ser evitada no pasto de ovelhas em pastejo.

TERMOS DE INDEXAÇÃO:
Protodioscina; Brachiaria spp.; ovinos; intoxicação por plantas; ruminantes; fotossensibilização hepatógena; fotodermatite; pastagem tropical; ruminante; saponinas esteroidais

Introduction

Plants of the genus Brachiaria are used in several countries as forage (Muniandy et al. 2020Muniandy K.V., Teik Chung E.L., Jaapar M.S., Mohd Hamdan M.H., Salleh A. & Abdullah Jesse F.F. 2020. Filling the gap of Brachiaria decumbens (signal grass) research on clinico-pathology and haemato-biochemistry in small ruminants: a review. Toxicon 174:26-31. <https://dx.doi.org/10.1016/j.toxicon.2019.12.158>
https://doi.org/10.1016/j.toxicon.2019.1...
) and cause spontaneous poisoning in cattle (Souza et al. 2010Souza R.I.C., Riet-Correa F., Brum K.B., Fernandes C.E., Barbosa-Ferreira M. & Lemos R.A.A. 2010. Intoxicação por Brachiaria spp. em bovinos no Mato Grosso do Sul. Pesq. Vet. Bras. 30(12):1036-1042. <https://dx.doi.org/10.1590/S0100-736X2010001200006>
https://doi.org/10.1590/S0100-736X201000...
, Riet-Correa et al. 2011Riet-Correa B., Castro M.B., Lemos R.A.A., Riet-Correa G., Mustafa V. & Riet-Correa F. 2011. Brachiaria spp. poisoning of ruminants in Brazil. Pesq. Vet. Bras. 31(3):183-192. <https://dx.doi.org/10.1590/S0100-736X2011000300001>
https://doi.org/10.1590/S0100-736X201100...
), sheep (Riet-Correa et al. 2011Riet-Correa B., Castro M.B., Lemos R.A.A., Riet-Correa G., Mustafa V. & Riet-Correa F. 2011. Brachiaria spp. poisoning of ruminants in Brazil. Pesq. Vet. Bras. 31(3):183-192. <https://dx.doi.org/10.1590/S0100-736X2011000300001>
https://doi.org/10.1590/S0100-736X201100...
, Faccin et al. 2014Faccin T.C., Riet-Correa F., Rodrigues F.S., Santos A.C., Melo G.K.A., Silva J.A., Ferreira R., Ítavo C.C.B.F. & Lemos R.A.A. 2014. Poisoning by Brachiaria brizantha in flocks of naïve and experienced sheep. Toxicon 82:1-8. <https://dx.doi.org/10.1016/j.toxicon.2014.02.008> <PMid:24561120>
https://doi.org/10.1016/j.toxicon.2014.0...
, Melo et al. 2018Melo G.K.A., Ítavo C.C.B.F., Silva J.A., Monteiro K.L.S., Faccin T.C., Pupin R.C., Heckler R.F., Ítavo L.C.V., Silva P.C.G., Leal P.V. & Lemos R.A.A. 2018. Poisoning by Brachiaria spp. in suckling lambs supplemented and unsupplemented in a creep-feeding system. Small Rumin. Res. 158:30-34. <https://dx.doi.org/10.1016/j.smallrumres.2017.11.014>
https://doi.org/10.1016/j.smallrumres.20...
, 2019aMelo G.K.A., Silva W.J., Pupin R.C., Heckler R.F., Nonato L.M., Ítavo C.C.B.F., Ferreira V.B.N. & Lemos R.A.A. 2019a. Comparison of two collection methods to determine protodioscin concentrations in Brachiaria spp. and to monitor Brachiaria spp. poisoning. Pesq. Vet. Bras. 39(9):710-714. <https://dx.doi.org/10.1590/1678-5150-PVB-6226>
https://doi.org/10.1590/1678-5150-PVB-62...
), goats (Rosa et al. 2016Rosa F.B., Rubin M.I.B., Martins T.B., Lemos R.A.A., Gomes D.C., Pupin R.C., Lima S.C. & Barros C.S.L. 2016. Spontaneous poisoning by Brachiaria decumbens in goats. Pesq. Vet. Bras. 36(5):389-396. <https://dx.doi.org/10.1590/S0100-736X2016000500006>
https://doi.org/10.1590/S0100-736X201600...
), buffaloes (De Oliveira et al. 2013De Oliveira C.H.S., Barbosa J.D., Oliveira C.M.C., Bastianetto E., Melo M.M., Haraguchi M., Freitas L.G.L., Silva M.X. & Leite R.C. 2013. Hepatic photosensitization in buffaloes intoxicated by Brachiaria decumbens in Minas Gerais state, Brazil. Toxicon 73:121-129. <https://dx.doi.org/10.1016/j.toxicon.2013.07.001> <PMid:23850427>
https://doi.org/10.1016/j.toxicon.2013.0...
), and horses (Barbosa et al. 2006Barbosa J.D., Oliveira C.M.C., Tokarnia C.H. & Peixoto P.V. 2006. Fotossensibilização hepatógena em equinos pela ingestão de Brachiaria humidicola (Graminae) no Estado do Pará. Pesq. Vet. Bras. 26(3):147-153. <https://dx.doi.org/10.1590/S0100-736X2006000300003>
https://doi.org/10.1590/S0100-736X200600...
). The poisoning was reproduced in sheep (Cruz et al. 2001Cruz C., Driemeier D., Pires V.S. & Schenkel E.P. 2001. Experimentally induced cholangiopathy by dosing sheep with fractionated extracts from Brachiaria decumbens. J. Vet. Diag. Invest. 13(2):170-172. <https://dx.doi.org/10.1177/104063870101300215> <PMid:11289217>
https://doi.org/10.1177/1040638701013002...
, Driemeier et al. 2002Driemeier D., Colodel E.M., Seitz A.L., Barros S.S. & Cruz C.E.F. 2002 Study of experimentally induced lesions in sheep by grazing Brachiaria decumbens. Toxicon 40(7):1027-1031. <https://dx.doi.org/10.1016/s0041-0101(01)00276-8> <PMid:12076657>
https://doi.org/10.1016/s0041-0101(01)00...
, Saturnino et al. 2010Saturnino K.C., Mariani T.M., Barbosa-Ferreira M., Brum K.B., Fernandes C.E.S. & Lemos R.A.A. 2010. Intoxicação experimental por Brachiaria decumbens em ovinos confinados. Pesq. Vet. Bras. 30(3):195-202. <https://dx.doi.org/10.1590/S0100-736X2010000300002>
https://doi.org/10.1590/S0100-736X201000...
, Porto et al. 2013Porto M.R., Saturnino K.C., Lima E.M.M., Lee S.T., Lemos R.A.A., Marcolongo-Pereira C., Riet-Correa F. & Castro M.B. 2013. Avaliação da exposição solar na intoxicação experimental por Brachiaria decumbens em ovinos. Pesq. Vet. Bras. 33(8):1009-1015. <https://dx.doi.org/10.1590/S0100-736X2013000800011>
https://doi.org/10.1590/S0100-736X201300...
), and rabbits (Utiumi et al. 2018Utiumi K.U., Albuquerque A.S., Burque A.S., Souza F.R., Sonne L., Varaschin M.S., Raymundo D.L. & Peconick A.P. 2018. Experimental poisoning by Brachiaria decumbens in rabbits. Pesq. Vet. Bras. 38(10):1885-1889. <https://dx.doi.org/10.1590/1678-5150-PVB-5599>
https://doi.org/10.1590/1678-5150-PVB-55...
). The main clinical presentation of the toxicosis in all livestock species is hepatogenous photosensitization (Riet-Correa et al. 2011Riet-Correa B., Castro M.B., Lemos R.A.A., Riet-Correa G., Mustafa V. & Riet-Correa F. 2011. Brachiaria spp. poisoning of ruminants in Brazil. Pesq. Vet. Bras. 31(3):183-192. <https://dx.doi.org/10.1590/S0100-736X2011000300001>
https://doi.org/10.1590/S0100-736X201100...
, Collett 2019Collett M.G. 2019. Photosensitisation diseases of animals: classification and a weight of evidence approach to primary causes. Toxicon X. 3:100012. <https://dx.doi.org/10.1016/j.toxcx.2019.100012> <PMid:32550569>
https://doi.org/10.1016/j.toxcx.2019.100...
). However, other syndromes are also associated with Brachiaria toxicosis, such as progressive weight loss and neurological disorders (Muniandy et al. 2020Muniandy K.V., Teik Chung E.L., Jaapar M.S., Mohd Hamdan M.H., Salleh A. & Abdullah Jesse F.F. 2020. Filling the gap of Brachiaria decumbens (signal grass) research on clinico-pathology and haemato-biochemistry in small ruminants: a review. Toxicon 174:26-31. <https://dx.doi.org/10.1016/j.toxicon.2019.12.158>
https://doi.org/10.1016/j.toxicon.2019.1...
).

The main toxic principle in Brachiaria spp. is protodioscin, which is present in higher concentrations in B. decumbens and in lower concentrations in the other cultivars of Brachiaria (Low 2015Low S.G. 2015. Signal grass (Brachiaria decumbens) toxicity in grazing ruminants. Agriculture 5:971-990. <https://dx.doi.org/10.3390/agriculture5040971>
https://doi.org/10.3390/agriculture50409...
, Lozano et al. 2017Lozano M., Martinez N. & Diaz G. 2017. Content of the saponin protodioscin in Brachiaria spp. from the Eastern Plains of Colombia. Toxins 9(7):220. <https://dx.doi.org/10.3390/toxins9070220> <PMid:28703748>
https://doi.org/10.3390/toxins9070220...
). However, the lack of standardization in the methodology for collecting forage samples for analysis makes it difficult to compare these concentrations and determine the toxic principle levels (Melo et al. 2018Melo G.K.A., Ítavo C.C.B.F., Silva J.A., Monteiro K.L.S., Faccin T.C., Pupin R.C., Heckler R.F., Ítavo L.C.V., Silva P.C.G., Leal P.V. & Lemos R.A.A. 2018. Poisoning by Brachiaria spp. in suckling lambs supplemented and unsupplemented in a creep-feeding system. Small Rumin. Res. 158:30-34. <https://dx.doi.org/10.1016/j.smallrumres.2017.11.014>
https://doi.org/10.1016/j.smallrumres.20...
). In addition to protodioscin levels in the pasture, other factors, such as the adaptation of animals (Faccin et al. 2014Faccin T.C., Riet-Correa F., Rodrigues F.S., Santos A.C., Melo G.K.A., Silva J.A., Ferreira R., Ítavo C.C.B.F. & Lemos R.A.A. 2014. Poisoning by Brachiaria brizantha in flocks of naïve and experienced sheep. Toxicon 82:1-8. <https://dx.doi.org/10.1016/j.toxicon.2014.02.008> <PMid:24561120>
https://doi.org/10.1016/j.toxicon.2014.0...
, Castro et al. 2018Castro M.B., Gracindo C.V., Landi M.F.A., Cabral Filho S.L.S., Resende Filho N.J., Lima E.M.M. & Riet-Correa F. 2018. Sheep adaptation management, and investigation of inherited resistance to prevent Brachiaria spp. poisoning. Small Rumin. Res. 158:42-47. <https://dx.doi.org/10.1016/j.smallrumres.2017.12.001>
https://doi.org/10.1016/j.smallrumres.20...
), age (Riet-Correa et al. 2011Riet-Correa B., Castro M.B., Lemos R.A.A., Riet-Correa G., Mustafa V. & Riet-Correa F. 2011. Brachiaria spp. poisoning of ruminants in Brazil. Pesq. Vet. Bras. 31(3):183-192. <https://dx.doi.org/10.1590/S0100-736X2011000300001>
https://doi.org/10.1590/S0100-736X201100...
, Muniandy et al. 2020Muniandy K.V., Teik Chung E.L., Jaapar M.S., Mohd Hamdan M.H., Salleh A. & Abdullah Jesse F.F. 2020. Filling the gap of Brachiaria decumbens (signal grass) research on clinico-pathology and haemato-biochemistry in small ruminants: a review. Toxicon 174:26-31. <https://dx.doi.org/10.1016/j.toxicon.2019.12.158>
https://doi.org/10.1016/j.toxicon.2019.1...
), genetic resistance (Pupin et al. 2016Pupin R.C., Melo G.K.A., Heckler R.F., Faccin T.C., Ítavo C.C.B.F., Fernandes C.E.C., Gomes D.C. & Lemos R.A.A. 2016. Identification of lamb flocks susceptible and resistant against Brachiaria poisoning. Pesq. Vet. Bras. 36(5):383-388. <https://dx.doi.org/10.1590/S0100-736X2016000500005>
https://doi.org/10.1590/S0100-736X201600...
), and animal species involved (Riet-Correa et al. 2011Riet-Correa B., Castro M.B., Lemos R.A.A., Riet-Correa G., Mustafa V. & Riet-Correa F. 2011. Brachiaria spp. poisoning of ruminants in Brazil. Pesq. Vet. Bras. 31(3):183-192. <https://dx.doi.org/10.1590/S0100-736X2011000300001>
https://doi.org/10.1590/S0100-736X201100...
, Lozano et al. 2017Lozano M., Martinez N. & Diaz G. 2017. Content of the saponin protodioscin in Brachiaria spp. from the Eastern Plains of Colombia. Toxins 9(7):220. <https://dx.doi.org/10.3390/toxins9070220> <PMid:28703748>
https://doi.org/10.3390/toxins9070220...
), affect the occurrence of poisoning.

Although various studies demonstrate that several species of Brachiaria induce poisoning, in some outbreaks, the sum of the ingestion of different species of Brachiaria spp. is responsible for the poisoning (Souza et al. 2010Souza R.I.C., Riet-Correa F., Brum K.B., Fernandes C.E., Barbosa-Ferreira M. & Lemos R.A.A. 2010. Intoxicação por Brachiaria spp. em bovinos no Mato Grosso do Sul. Pesq. Vet. Bras. 30(12):1036-1042. <https://dx.doi.org/10.1590/S0100-736X2010001200006>
https://doi.org/10.1590/S0100-736X201000...
, Ogliari et al. 2018Ogliari D., Molossi F.A., Savaris T., Wicpolt N.S., Zacan I. & Gava A. 2018. Intoxicação espontânea por Brachiaria híbrida cv mulato I em ovinos e caprinos e experimental por Brachiaria híbrida cv mulato II em ovinos. Pesq. Vet. Bras. 38(2):229-233. <https://dx.doi.org/10.1590/1678-5150-PVB-4747>
https://doi.org/10.1590/1678-5150-PVB-47...
). In those instances, the protodioscin concentrations were not determined (Lemos et al. 1996Lemos R.A.A., Ferreira L.C.L., Silva S.M., Nakazato L. & Salvador S.C. 1996. Fotossensibilização e colangiopatia associada a cristais em ovinos em pastagem com Brachiaria decumbens. Ciência Rural 26(1):109-113. <https://dx.doi.org/10.1590/S0103-84781996000100020>
https://doi.org/10.1590/S0103-8478199600...
, Caicedo et al. 2012Caicedo J.A., Ospina J.C., Chaves C.A., Peña J., Lozano M.C. & Doncel B. 2012. Hepatic lesions in cattle grazing on Brachiaria decumbens in Mesatas, Meta (Colombia). Revta Med. Vet. Zootec. 59(2):102-108., Rosa et al. 2016Rosa F.B., Rubin M.I.B., Martins T.B., Lemos R.A.A., Gomes D.C., Pupin R.C., Lima S.C. & Barros C.S.L. 2016. Spontaneous poisoning by Brachiaria decumbens in goats. Pesq. Vet. Bras. 36(5):389-396. <https://dx.doi.org/10.1590/S0100-736X2016000500006>
https://doi.org/10.1590/S0100-736X201600...
, Utiumi et al. 2018Utiumi K.U., Albuquerque A.S., Burque A.S., Souza F.R., Sonne L., Varaschin M.S., Raymundo D.L. & Peconick A.P. 2018. Experimental poisoning by Brachiaria decumbens in rabbits. Pesq. Vet. Bras. 38(10):1885-1889. <https://dx.doi.org/10.1590/1678-5150-PVB-5599>
https://doi.org/10.1590/1678-5150-PVB-55...
), and even when they were, each plant species was not analyzed separately (Mustafa et al. 2012Mustafa V.S., Moscardini A.R.C., Borges J.R.J., Reckziegel G.C., Riet-Correa F. & Castro M.B. 2012. Intoxicação natural por Brachiaria spp. em ovinos no Brasil Central. Pesq. Vet. Bras. 32(12):1272-1280. <https://dx.doi.org/10.1590/S0100-736X2012001200010>
https://doi.org/10.1590/S0100-736X201200...
, Diamantino et al. 2018Diamantino G.M.L., Biscoto G.L., Pedroza H.P., Amorim R.N.L., Keller K.M., Melo M.M. & Soto-Blanco B. 2018. Liquid chromatography coupled to quadrupole time-of-flight- mass spectrometry (QTOF/MS) assay for quantification of protodioscina in Brachiaria grasses. Toxicon 155:61-65. <https://dx.doi.org/10.1016/j.toxicon.2018.10.008>
https://doi.org/10.1016/j.toxicon.2018.1...
, Melo et al. 2018Melo G.K.A., Ítavo C.C.B.F., Silva J.A., Monteiro K.L.S., Faccin T.C., Pupin R.C., Heckler R.F., Ítavo L.C.V., Silva P.C.G., Leal P.V. & Lemos R.A.A. 2018. Poisoning by Brachiaria spp. in suckling lambs supplemented and unsupplemented in a creep-feeding system. Small Rumin. Res. 158:30-34. <https://dx.doi.org/10.1016/j.smallrumres.2017.11.014>
https://doi.org/10.1016/j.smallrumres.20...
, 2019aMelo G.K.A., Silva W.J., Pupin R.C., Heckler R.F., Nonato L.M., Ítavo C.C.B.F., Ferreira V.B.N. & Lemos R.A.A. 2019a. Comparison of two collection methods to determine protodioscin concentrations in Brachiaria spp. and to monitor Brachiaria spp. poisoning. Pesq. Vet. Bras. 39(9):710-714. <https://dx.doi.org/10.1590/1678-5150-PVB-6226>
https://doi.org/10.1590/1678-5150-PVB-62...
, 2019bMelo G.K.A., Silva W.J., Pupin R.C., Heckler R.F., Nonato L.M., Ítavo C.C.B.F., Ferreira V.B.N. & Lemos R.A.A. 2019b. Poisoning by Brachiaria spp. In various lamb breeds at increasing levels of supplementation during growth. Pesq. Vet. Bras. 39(12):978-982. <https://dx.doi.org/10.1590/1678-5150-PVB-6478>
https://doi.org/10.1590/1678-5150-PVB-64...
).

The main objective of this study was to evaluate the levels of protodioscin in B. decumbens and B. brizantha in pastures where Brachiaria poisoning in sheep occurred. We also review the literature on the concentrations and methodologies of sampling of the plant and analysis of the toxic principle and evaluate the risk of infestation of the pastures by more toxic plant species, in facilitating the occurrence of poisoning by plants of this genus in ruminants.

Materials and Methods

The study was approved by the Ethics Committee on the Use of Animals of the “Universidade Federal de Mato Grosso do Sul” (UFMS), protocol number 0862/2017.

The experiment was carried out within the experimental area of the “Fazenda Escola” of the UFMS (20°26’34.31” South and 54°50’27.86” West, 530.7m altitude) from November 2018 to April 2019. The region is a rainy tropical savanna, subtype Aw, with seasonal rainfall distribution. The experimental period was in the most significant annual rainfall period, with an average temperature of 25.4°C and an accumulated rainfall of 829.7mm (INMET 2018INMET 2018. Instituto Nacional de Meteorologia, Ministério da Agricultura Pecuária e Abastecimento. Available at <Available at www.agraer.ms.gov.br/cemtec > Accessed on Jun. 2018.
www.agraer.ms.gov.br/cemtec...
).

Brachiaria brizantha originally formed the pastures, which were later invaded by many spots of Brachiaria decumbens. These pastures were occupied in previous years by sheep that developed poisoning with Brachiaria spp. (Pupin et al. 2016Pupin R.C., Melo G.K.A., Heckler R.F., Faccin T.C., Ítavo C.C.B.F., Fernandes C.E.C., Gomes D.C. & Lemos R.A.A. 2016. Identification of lamb flocks susceptible and resistant against Brachiaria poisoning. Pesq. Vet. Bras. 36(5):383-388. <https://dx.doi.org/10.1590/S0100-736X2016000500005>
https://doi.org/10.1590/S0100-736X201600...
, Melo et al. 2018Melo G.K.A., Ítavo C.C.B.F., Silva J.A., Monteiro K.L.S., Faccin T.C., Pupin R.C., Heckler R.F., Ítavo L.C.V., Silva P.C.G., Leal P.V. & Lemos R.A.A. 2018. Poisoning by Brachiaria spp. in suckling lambs supplemented and unsupplemented in a creep-feeding system. Small Rumin. Res. 158:30-34. <https://dx.doi.org/10.1016/j.smallrumres.2017.11.014>
https://doi.org/10.1016/j.smallrumres.20...
, 2019aMelo G.K.A., Silva W.J., Pupin R.C., Heckler R.F., Nonato L.M., Ítavo C.C.B.F., Ferreira V.B.N. & Lemos R.A.A. 2019a. Comparison of two collection methods to determine protodioscin concentrations in Brachiaria spp. and to monitor Brachiaria spp. poisoning. Pesq. Vet. Bras. 39(9):710-714. <https://dx.doi.org/10.1590/1678-5150-PVB-6226>
https://doi.org/10.1590/1678-5150-PVB-62...
). The grazing areas had drinking fountains and a small covered area with free access for night shelter and protection against eventual rainfalls or intense sunlight exposure.

The flock was initially composed of 69 lambs born to fathers and mothers adapted to the consumption of pastures formed by the Brachiaria spp. The criterion used to consider an adapted or resistant sheep was the absence of clinical signs throughout its lifespan, even when kept in pastures made up exclusively of Brachiaria spp. (Gracindo et al. 2014Gracindo C.V., Louvandini H., Riet-Correa F., Barbosa-Ferreira M. & Castro M.B. 2014. Performance of sheep grazing in pastures of Brachiaria decumbens, Brachiaria brizantha, Panicum maximum, and Andropogon gayanus with different protodioscin concentrations. Trop. Anim. Health Prod. 46(5):733-737. <https://dx.doi.org/10.1007/s11250-014-0556-y> <PMid:24557590>
https://doi.org/10.1007/s11250-014-0556-...
, Pupin et al. 2016Pupin R.C., Melo G.K.A., Heckler R.F., Faccin T.C., Ítavo C.C.B.F., Fernandes C.E.C., Gomes D.C. & Lemos R.A.A. 2016. Identification of lamb flocks susceptible and resistant against Brachiaria poisoning. Pesq. Vet. Bras. 36(5):383-388. <https://dx.doi.org/10.1590/S0100-736X2016000500005>
https://doi.org/10.1590/S0100-736X201600...
, Melo et al. 2019aMelo G.K.A., Silva W.J., Pupin R.C., Heckler R.F., Nonato L.M., Ítavo C.C.B.F., Ferreira V.B.N. & Lemos R.A.A. 2019a. Comparison of two collection methods to determine protodioscin concentrations in Brachiaria spp. and to monitor Brachiaria spp. poisoning. Pesq. Vet. Bras. 39(9):710-714. <https://dx.doi.org/10.1590/1678-5150-PVB-6226>
https://doi.org/10.1590/1678-5150-PVB-62...
). The ram breeder of the herd was supposedly adapted. However, it has a family history of illness and death due to Brachiaria spp. poisoning.

The grazing method lambs were managed with continuous stocking and variable stocking rate, supplemented daily with mineral supplement and energy protein supplement. The sheep were identified with earrings and necklaces and dewormed with 1ml/10kg of oral closantel 10 days before the beginning of the experiment.

The sheep were observed daily for clinical signs described for Brachiaria spp. poisoning. These include edema, erythema, and crusts in the non-pigmented areas of the face and ears, apathy, anorexia, and jaundice (Mustafa et al. 2012Mustafa V.S., Moscardini A.R.C., Borges J.R.J., Reckziegel G.C., Riet-Correa F. & Castro M.B. 2012. Intoxicação natural por Brachiaria spp. em ovinos no Brasil Central. Pesq. Vet. Bras. 32(12):1272-1280. <https://dx.doi.org/10.1590/S0100-736X2012001200010>
https://doi.org/10.1590/S0100-736X201200...
, Porto et al. 2013Porto M.R., Saturnino K.C., Lima E.M.M., Lee S.T., Lemos R.A.A., Marcolongo-Pereira C., Riet-Correa F. & Castro M.B. 2013. Avaliação da exposição solar na intoxicação experimental por Brachiaria decumbens em ovinos. Pesq. Vet. Bras. 33(8):1009-1015. <https://dx.doi.org/10.1590/S0100-736X2013000800011>
https://doi.org/10.1590/S0100-736X201300...
, Faccin et al. 2014Faccin T.C., Riet-Correa F., Rodrigues F.S., Santos A.C., Melo G.K.A., Silva J.A., Ferreira R., Ítavo C.C.B.F. & Lemos R.A.A. 2014. Poisoning by Brachiaria brizantha in flocks of naïve and experienced sheep. Toxicon 82:1-8. <https://dx.doi.org/10.1016/j.toxicon.2014.02.008> <PMid:24561120>
https://doi.org/10.1016/j.toxicon.2014.0...
, Pupin et al. 2016Pupin R.C., Melo G.K.A., Heckler R.F., Faccin T.C., Ítavo C.C.B.F., Fernandes C.E.C., Gomes D.C. & Lemos R.A.A. 2016. Identification of lamb flocks susceptible and resistant against Brachiaria poisoning. Pesq. Vet. Bras. 36(5):383-388. <https://dx.doi.org/10.1590/S0100-736X2016000500005>
https://doi.org/10.1590/S0100-736X201600...
, Melo et al. 2018Melo G.K.A., Ítavo C.C.B.F., Silva J.A., Monteiro K.L.S., Faccin T.C., Pupin R.C., Heckler R.F., Ítavo L.C.V., Silva P.C.G., Leal P.V. & Lemos R.A.A. 2018. Poisoning by Brachiaria spp. in suckling lambs supplemented and unsupplemented in a creep-feeding system. Small Rumin. Res. 158:30-34. <https://dx.doi.org/10.1016/j.smallrumres.2017.11.014>
https://doi.org/10.1016/j.smallrumres.20...
, 2019aMelo G.K.A., Silva W.J., Pupin R.C., Heckler R.F., Nonato L.M., Ítavo C.C.B.F., Ferreira V.B.N. & Lemos R.A.A. 2019a. Comparison of two collection methods to determine protodioscin concentrations in Brachiaria spp. and to monitor Brachiaria spp. poisoning. Pesq. Vet. Bras. 39(9):710-714. <https://dx.doi.org/10.1590/1678-5150-PVB-6226>
https://doi.org/10.1590/1678-5150-PVB-62...
). When those signs were spotted in any lamb, it underwent thorough clinical examinations and immediately removed from the lot, kept in stalls sheltered from sunlight, consuming mineral salt, energy-based protein concentrate soybean meal, and crushed corn fresh millet and water ad libitum. In fatal cases, a necropsy was performed, and fragments of several organs were collected in 10% formalin solution for histopathological processing routine staining by the hematoxylin and eosin (HE) technique. The occurrence of poisoning cases by Brachiaria spp. was a criterion for confirming pasture toxicity.

Five Brachiaria samples were collected from the paddocks at intervals of every 28 days by manual grazing simulation (Cook 1964Cook C.W. 1964. Collecting forage samples representative of ingested material of grazing animals for nutritional studies. Anim. Sci. J. 23(1):265-270. <https://dx.doi.org/10.2527/jas1964.231265x>
https://doi.org/10.2527/jas1964.231265x...
). Before sampling, we observed the sheep grazing behavior location and forage proportion, with an average of ten different locations in each paddock, to obtain a sample of the plant similar to that selected by the lambs. Samples were also collected from the mixed pasture of Brachiaria spp. (cv. Maranda and cv. Basilisk) and samples of each cultivar.

After collection, the samples were weighed and dried at 55°C for 72 h, ground in a mill with a 1-mm sieve screen, and stored. They were then analyzed to detect protodioscin using high-performance liquid chromatography-electrospray ionization mass spectrometry (HPLC-ESI-MS), as previously described (Lee et al. 2009Lee S.T., Mitchell R.B., Wang Z., Heiss C., Gardner D.R. & Azadi P. 2009. Isolation, characaterization, and quantification of steroidal saponins in switchgrass (Panicum Virgatum L.). J. Agric. Food. Chem. 57(6):2599-2604. <https://dx.doi.org/10.1021/jf803907y> <PMid:19243100>
https://doi.org/10.1021/jf803907y...
).

Results

There was a predilection for the sheep to graze areas that contained Brachiaria decumbens over Brachiaria brizantha. After consuming all the grass of their first choice, they then went on to consume B. brizantha.

Five sheep got sick, three died, and two recovered. At necropsy of the three sheep, the observed changes were similar and varied only in severity. Jaundice was consistent in the ocular and oral mucosa, subcutaneous tissue, omentum, and arteries’ intima. The liver was diffusely yellow-brown with a marked lobular pattern; there was a coppery hue to the kidneys’ cortex.

Histologically, there was moderate hyperplasia of the hepatic bile ducts, which had their lumina distended and filled by negative images of birefringent acicular crystals. A minimal lymphocytic infiltration was the periportal regions. In the centrilobular and periportal areas, there were abundant clusters of macrophages with abundant foamy cytoplasm. Occasionally, in the centrilobular regions, individual hepatocellular necrosis was observed. Cholestasis was also a consistent finding.

The levels of protodioscin found in the samples of the evaluated paddocks ranged from 0.70 to 1.45%, and when the species were analyzed separately, higher levels were observed in B. decumbens (7.09%) than B. brizantha (1.04%).

The epidemiological data and protodioscin concentrations from previous studies are given in Table 1 and 2.

Table 1.
Data on several outbreaks of Brachiaria spp. poisoning in ruminants
Table 2.
Brachiaria spp. poisoning in ruminants. Determination of the levels of protodioscin in the plant and methods of sampling

Discussion

Pasture toxicity was determined by the occurrence of cases with clinical and pathological features of Brachiaria spp. poisoning (Mustafa et al. 2012Mustafa V.S., Moscardini A.R.C., Borges J.R.J., Reckziegel G.C., Riet-Correa F. & Castro M.B. 2012. Intoxicação natural por Brachiaria spp. em ovinos no Brasil Central. Pesq. Vet. Bras. 32(12):1272-1280. <https://dx.doi.org/10.1590/S0100-736X2012001200010>
https://doi.org/10.1590/S0100-736X201200...
, Porto et al. 2013Porto M.R., Saturnino K.C., Lima E.M.M., Lee S.T., Lemos R.A.A., Marcolongo-Pereira C., Riet-Correa F. & Castro M.B. 2013. Avaliação da exposição solar na intoxicação experimental por Brachiaria decumbens em ovinos. Pesq. Vet. Bras. 33(8):1009-1015. <https://dx.doi.org/10.1590/S0100-736X2013000800011>
https://doi.org/10.1590/S0100-736X201300...
, Faccin et al. 2014Faccin T.C., Riet-Correa F., Rodrigues F.S., Santos A.C., Melo G.K.A., Silva J.A., Ferreira R., Ítavo C.C.B.F. & Lemos R.A.A. 2014. Poisoning by Brachiaria brizantha in flocks of naïve and experienced sheep. Toxicon 82:1-8. <https://dx.doi.org/10.1016/j.toxicon.2014.02.008> <PMid:24561120>
https://doi.org/10.1016/j.toxicon.2014.0...
, Pupin et al. 2016Pupin R.C., Melo G.K.A., Heckler R.F., Faccin T.C., Ítavo C.C.B.F., Fernandes C.E.C., Gomes D.C. & Lemos R.A.A. 2016. Identification of lamb flocks susceptible and resistant against Brachiaria poisoning. Pesq. Vet. Bras. 36(5):383-388. <https://dx.doi.org/10.1590/S0100-736X2016000500005>
https://doi.org/10.1590/S0100-736X201600...
, Melo et al. 2018Melo G.K.A., Ítavo C.C.B.F., Silva J.A., Monteiro K.L.S., Faccin T.C., Pupin R.C., Heckler R.F., Ítavo L.C.V., Silva P.C.G., Leal P.V. & Lemos R.A.A. 2018. Poisoning by Brachiaria spp. in suckling lambs supplemented and unsupplemented in a creep-feeding system. Small Rumin. Res. 158:30-34. <https://dx.doi.org/10.1016/j.smallrumres.2017.11.014>
https://doi.org/10.1016/j.smallrumres.20...
, 2019aMelo G.K.A., Silva W.J., Pupin R.C., Heckler R.F., Nonato L.M., Ítavo C.C.B.F., Ferreira V.B.N. & Lemos R.A.A. 2019a. Comparison of two collection methods to determine protodioscin concentrations in Brachiaria spp. and to monitor Brachiaria spp. poisoning. Pesq. Vet. Bras. 39(9):710-714. <https://dx.doi.org/10.1590/1678-5150-PVB-6226>
https://doi.org/10.1590/1678-5150-PVB-62...
). The pasture where the sheep were grazing was previously reported as toxic (Faccin et al. 2014Faccin T.C., Riet-Correa F., Rodrigues F.S., Santos A.C., Melo G.K.A., Silva J.A., Ferreira R., Ítavo C.C.B.F. & Lemos R.A.A. 2014. Poisoning by Brachiaria brizantha in flocks of naïve and experienced sheep. Toxicon 82:1-8. <https://dx.doi.org/10.1016/j.toxicon.2014.02.008> <PMid:24561120>
https://doi.org/10.1016/j.toxicon.2014.0...
, Melo et al. 2019aMelo G.K.A., Silva W.J., Pupin R.C., Heckler R.F., Nonato L.M., Ítavo C.C.B.F., Ferreira V.B.N. & Lemos R.A.A. 2019a. Comparison of two collection methods to determine protodioscin concentrations in Brachiaria spp. and to monitor Brachiaria spp. poisoning. Pesq. Vet. Bras. 39(9):710-714. <https://dx.doi.org/10.1590/1678-5150-PVB-6226>
https://doi.org/10.1590/1678-5150-PVB-62...
). However, in these previous reports, only Brachiaria brizantha was considered since the pasture had been formed using seeds of this type of forage. Although it was not possible to quantitatively assess the presence of Brachiaria decumbens, the possibility of contamination of the seeds or even the invasion of pasture by this other species cannot be ruled out in previous outbreaks.

B. decumbens in pasture and the preference of sheep for its consumption over B. brizantha, as observed in the current study, shows that the introduction of sheep in paddocks where this forage is present is a high-risk factor for the poisoning. This fact is even more relevant if we consider that the poisoning occurred in a herd consisting of sheep considered resistant to the ill-effects of Brachiaria spp.

The fact that a ram with no history of Brachiaria spp. poisoning can transmit vulnerability to poisoning to their offspring is a limiting factor for selecting resistant herds since the main criterion adopted for this selection is the culling of animals that show clinical signs of poisoning (Faccin et al. 2014Faccin T.C., Riet-Correa F., Rodrigues F.S., Santos A.C., Melo G.K.A., Silva J.A., Ferreira R., Ítavo C.C.B.F. & Lemos R.A.A. 2014. Poisoning by Brachiaria brizantha in flocks of naïve and experienced sheep. Toxicon 82:1-8. <https://dx.doi.org/10.1016/j.toxicon.2014.02.008> <PMid:24561120>
https://doi.org/10.1016/j.toxicon.2014.0...
). This criterion is efficient in herds with well-defined zootechnical and sanitary standards. However, it does not apply to breeding sheep, mainly when they are from places where forages of Brachiaria are absent from the pastures. Considering that young sheep are more sensitive (Muniandy et al. 2020Muniandy K.V., Teik Chung E.L., Jaapar M.S., Mohd Hamdan M.H., Salleh A. & Abdullah Jesse F.F. 2020. Filling the gap of Brachiaria decumbens (signal grass) research on clinico-pathology and haemato-biochemistry in small ruminants: a review. Toxicon 174:26-31. <https://dx.doi.org/10.1016/j.toxicon.2019.12.158>
https://doi.org/10.1016/j.toxicon.2019.1...
) and breeders are acquired as adults, the criterion of the absence of clinical signs of poisoning in breeders is not a guarantee of resistance in their offspring.

This study has four key findings: (i) a difference in the concentration of protodioscin between the two Brachiaria species was observed; (ii) sheep show a preference for B. decumbens; (iii) the characterization of the composition of the pasture; and (iv) the stratified analysis of the concentrations of the toxic principle in both plant species should be done as standard in cases of outbreaks or studies on the toxicity of Brachiaria spp.

As shown in Table 1, the comparison of protodioscin concentrations in samples of plants of the genus Brachiaria that are toxic to sheep is hampered by the lack of standardization in collecting samples. Although B. decumbens is considered the most toxic among the species (Riet-Correa et al. 2011Riet-Correa B., Castro M.B., Lemos R.A.A., Riet-Correa G., Mustafa V. & Riet-Correa F. 2011. Brachiaria spp. poisoning of ruminants in Brazil. Pesq. Vet. Bras. 31(3):183-192. <https://dx.doi.org/10.1590/S0100-736X2011000300001>
https://doi.org/10.1590/S0100-736X201100...
), its highest concentration of the toxic principle described so far was 3.54%, in the plant’s maturation phase (De Oliveira et al. 2013De Oliveira C.H.S., Barbosa J.D., Oliveira C.M.C., Bastianetto E., Melo M.M., Haraguchi M., Freitas L.G.L., Silva M.X. & Leite R.C. 2013. Hepatic photosensitization in buffaloes intoxicated by Brachiaria decumbens in Minas Gerais state, Brazil. Toxicon 73:121-129. <https://dx.doi.org/10.1016/j.toxicon.2013.07.001> <PMid:23850427>
https://doi.org/10.1016/j.toxicon.2013.0...
). The vegetative stage has a strong influence on protodioscin concentrations, which are higher in sprouting and decrease as they mature (Castro et al. 2011Castro M.B., Santos Jr. H.L., Mustafa V.S., Gracindo C.V., Moscardini A.C.R., Louvandini H., Paludo G.R., Borges J.R.J., Haraguchi M., Ferreira M.B. & Riet-Correa F. 2011. Brachiaria spp. poisoning in sheep in Brazil: experimental and epidemiological findings, p.110-117. In: Riet-Correa F., Pfister J., Schild A.L. & Wierenga T. (Eds), Poisoning by Plants, Mycotoxins and Related Toxins. CAB International, London., Ferreira et al. 2011Ferreira M.B., Brum K.B., Fernandes C.E., Martins C.F., Pinto G.S., Castro V.S., Rezende K.G., Riet-Correa F., Haraguchi M., Wysocki H.L. & Lemos R.A.A. 2011. Variation in saponin concentration in Brachiaria brizantha leaves as a function of maturation: preliminar data, p.118-123. In: Riet-Correa F., Pfister J., Schild A.L. & Wierenga T.L. (Eds), Poisoning by Plants, Mycotoxins and Related Toxins. CAB International, Wallingford., Riet-Correa et al. 2011Riet-Correa B., Castro M.B., Lemos R.A.A., Riet-Correa G., Mustafa V. & Riet-Correa F. 2011. Brachiaria spp. poisoning of ruminants in Brazil. Pesq. Vet. Bras. 31(3):183-192. <https://dx.doi.org/10.1590/S0100-736X2011000300001>
https://doi.org/10.1590/S0100-736X201100...
, Lima et al. 2012Lima F.G.D., Haraguchi M., Pifster J.A., Guimarães V.Y., Andrade D.F., Ribeiro C.S., Costa G.L., Araujo A.L.L. & Fioravanti M.C.S. 2012. Weather and plant age affect the levels of steroidal saponin and Pithomyces chartarum spores in Brachiaria grass. Int. J. Poisonous Plant Res. 2:45-53.), as seen in hay samples (Lima et al. 2012Lima F.G.D., Haraguchi M., Pifster J.A., Guimarães V.Y., Andrade D.F., Ribeiro C.S., Costa G.L., Araujo A.L.L. & Fioravanti M.C.S. 2012. Weather and plant age affect the levels of steroidal saponin and Pithomyces chartarum spores in Brachiaria grass. Int. J. Poisonous Plant Res. 2:45-53., Lozano et al. 2017Lozano M., Martinez N. & Diaz G. 2017. Content of the saponin protodioscin in Brachiaria spp. from the Eastern Plains of Colombia. Toxins 9(7):220. <https://dx.doi.org/10.3390/toxins9070220> <PMid:28703748>
https://doi.org/10.3390/toxins9070220...
).

Thus, the collection methodology must consider the animals’ feeding habits, as there may be differences in pasture consumption between species. Sheep, for example, have a preference for sprouts and, therefore, it may be that they consume higher levels of the toxic principle (Melo et al. 2019aMelo G.K.A., Silva W.J., Pupin R.C., Heckler R.F., Nonato L.M., Ítavo C.C.B.F., Ferreira V.B.N. & Lemos R.A.A. 2019a. Comparison of two collection methods to determine protodioscin concentrations in Brachiaria spp. and to monitor Brachiaria spp. poisoning. Pesq. Vet. Bras. 39(9):710-714. <https://dx.doi.org/10.1590/1678-5150-PVB-6226>
https://doi.org/10.1590/1678-5150-PVB-62...
). In addition to the higher concentrations of protodioscin in B. decumbens compared to B. brizantha (Lima et al. 2012Lima F.G.D., Haraguchi M., Pifster J.A., Guimarães V.Y., Andrade D.F., Ribeiro C.S., Costa G.L., Araujo A.L.L. & Fioravanti M.C.S. 2012. Weather and plant age affect the levels of steroidal saponin and Pithomyces chartarum spores in Brachiaria grass. Int. J. Poisonous Plant Res. 2:45-53., Lozano et al. 2017Lozano M., Martinez N. & Diaz G. 2017. Content of the saponin protodioscin in Brachiaria spp. from the Eastern Plains of Colombia. Toxins 9(7):220. <https://dx.doi.org/10.3390/toxins9070220> <PMid:28703748>
https://doi.org/10.3390/toxins9070220...
), the more significant toxicity of the former is corroborated by the greater numbers of outbreaks caused by B. decumbens poisoning, even when the proportion of B. brizantha in the pasture is higher (Riet-Correa et al. 2011Riet-Correa B., Castro M.B., Lemos R.A.A., Riet-Correa G., Mustafa V. & Riet-Correa F. 2011. Brachiaria spp. poisoning of ruminants in Brazil. Pesq. Vet. Bras. 31(3):183-192. <https://dx.doi.org/10.1590/S0100-736X2011000300001>
https://doi.org/10.1590/S0100-736X201100...
).

Considering only the analyzes of B. decumbens carried out in the present study, the values are higher than those found in all previous evaluations of this and other Brachiaria species, even using different collection methodologies, indicating that this species is responsible for the cases of Brachiaria poisoning in the sheep of the current study. A relevant fact is that in a study carried out in the same area of the present study and using a similar sampling methodology, without considering the invasion by B. decumbens, protodioscin levels ranged from 0.42% to 1.81% (Melo et al. 2019aMelo G.K.A., Silva W.J., Pupin R.C., Heckler R.F., Nonato L.M., Ítavo C.C.B.F., Ferreira V.B.N. & Lemos R.A.A. 2019a. Comparison of two collection methods to determine protodioscin concentrations in Brachiaria spp. and to monitor Brachiaria spp. poisoning. Pesq. Vet. Bras. 39(9):710-714. <https://dx.doi.org/10.1590/1678-5150-PVB-6226>
https://doi.org/10.1590/1678-5150-PVB-62...
). These results, added to the sheep’s predilection for consuming this plant, show that one should not use the forage to feed sheep even when mixed with another forage.

It is noteworthy that the presence of protodioscin concentrations is not the only risk factor for poisoning. Another critical risk factor to be considered is the introduction of a breeder with a family history of the occurrence of poisoning. Previous studies have demonstrated the importance of genetics for sensitivity and resistance to poisoning (Pupin et al. 2016Pupin R.C., Melo G.K.A., Heckler R.F., Faccin T.C., Ítavo C.C.B.F., Fernandes C.E.C., Gomes D.C. & Lemos R.A.A. 2016. Identification of lamb flocks susceptible and resistant against Brachiaria poisoning. Pesq. Vet. Bras. 36(5):383-388. <https://dx.doi.org/10.1590/S0100-736X2016000500005>
https://doi.org/10.1590/S0100-736X201600...
) and the higher occurrence of resistant lambs born to a particular breeder, who during his lifetime did not show signs of poisoning (Melo et al. 2018Melo G.K.A., Ítavo C.C.B.F., Silva J.A., Monteiro K.L.S., Faccin T.C., Pupin R.C., Heckler R.F., Ítavo L.C.V., Silva P.C.G., Leal P.V. & Lemos R.A.A. 2018. Poisoning by Brachiaria spp. in suckling lambs supplemented and unsupplemented in a creep-feeding system. Small Rumin. Res. 158:30-34. <https://dx.doi.org/10.1016/j.smallrumres.2017.11.014>
https://doi.org/10.1016/j.smallrumres.20...
).

Conclusions

The concentrations of protodioscin in Brachiaria decumbens may be much higher than the levels considered to be a risk for the occurrence of poisoning in sheep.

The difference between the concentrations of protodioscin observed in B. decumbens and Brachiaria brizantha in the pasture, and the preference of the sheep for the first indicates that the methods for the analysis of the toxic principle in Brachiaria spp. in studies of the toxicity and must include botanical identification and separately chemical species analysis.

Acknowledgments

Three of the authors (R.A.A. Lemos, G.S. Difante and C.C.B.F Ítavo) have research fellowships from the “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq). This work was carried out with the support of the “Coordenação de Aperfeiçoamento de Pessoa de Nível Superior” (CAPES), Brazil - Financing Code 001. The authors were supported by the “Universidade Federal de Mato Grosso do Sul” (UFMS) and “Fundação para o Desenvolvimento da Educação, Ciência e Tecnologia do Estado do Mato Grosso do Sul” (FUNDECT).

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Publication Dates

  • Publication in this collection
    23 July 2021
  • Date of issue
    2021

History

  • Received
    15 May 2021
  • Accepted
    28 May 2021
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