Theileria sp. in water buffaloes from Maranhão State, northeastern Brazil

Theileria sp. em búfalos do Estado do Maranhão, nordeste do Brasil

Hugo Luca Abate Nelson Jessé Rodrigues dos Santos Danilo Rodrigues Barros Brito Jessica Damiana Marinho Valente Thállitha Samih Wischral Jayme Vieira João Luis Garcia Rafael Felipe da Costa Vieira Odilon Vidotto About the authors

Abstract

Anaplasma marginale and piroplasm species are widespread among Brazilian cattle herds. Both of these tick-borne pathogens hamper livestock production and cause a significant economic impact. Although buffaloes have demonstrated a high level of adaptability, data on tick-borne pathogens are scarcely reported in Brazil. Thus, the aim of this study was to screen water buffaloes from the state of Maranhão for piroplasm and A. marginale occurrence using PCR assays. All samples were negative for A. marginale. One of the 287 (0.35%) water buffaloes tested was positive for Theileria sp. Sequencing of the 18S rDNA fragment (356 bp) showed that the Theileria sp. identified was closely related to the T. buffeli /orientalis group. Future studies on the clinical signs of infection and the main vector in this country are needed.

Keywords:
Piroplasms; Anaplasma marginale; ticks; PCR

Resumo

Anaplasma marginale e espécies de piroplasma são amplamente distribuídas no rebanho bovino brasileiro. Ambos os patógenos transmitidos por carrapatos dificultam a produção pecuária e causam um impacto econômico significativo. Embora os búfalos tenham demonstrado um alto nível de adaptabilidade, dados sobre patógenos transmitidos por carrapatos são raramente relatados no Brasil. Assim, o objetivo deste estudo foi investigar búfalos do estado do Maranhão para piroplasmas e A. marginale utilizando-se a técnica da PCR. Todas as amostras foram negativas para A. marginale . Um dos 287 (0,35%) búfalos testados foi positivo para Theileria sp. O sequenciamento de um fragmento do gene 18S rDNA (356 pb) demonstrou que Theileria sp. identificado estava relacionada ao grupo T. buffeli/orientalis . Estudos futuros sobre os sinais clínicos de infecção e o principal vetor neste país são necessários.

Palavras-chave:
Piroplasmas; Anaplasma marginale; carrapatos; PCR

Bovine piroplasmosis, caused by Babesia spp. and Theileria spp., is a tick-borne protozoan disease that infects cattle and buffaloes worldwide ( SIVAKUMAR et al., 2014 Sivakumar T, Tattiyapong M, Fukushi S, Hayashida K, Kothalawala H, Silva SS, et al. Genetic characterization of Babesia and Theileria parasites in water buffaloes in Sri Lanka. Vet Parasitol 2014; 200(1-2): 24-30. http://dx.doi.org/10.1016/j.vetpar.2013.11.029. PMid:24365246.
http://dx.doi.org/10.1016/j.vetpar.2013...
). Babesia bovis, B. bigemina, Theileria parva, and T. annulata are known to have a significant impact on the cattle industry ( BOCK et al., 2004 Bock R, Jackson L, Vos A, Jorgensen W. Babesiosis of cattle. Parasitology 2004;129(Suppl. 1): 247-269. http://dx.doi.org/10.1017/S0031182004005190. PMid:15938514.
http://dx.doi.org/10.1017/S003118200400...
). Although clinical manifestations are not commonly observed in piroplasm-infected water buffaloes (Bubalus bubalis) ( VINODKUMAR et al., 2016 Vinodkumar K, Shyma V, Justin DK, Ashok S, Anu JP, Mini K, et al. Fatal Theileria orientalis N2 genotype infection among Asian water buffaloes (Bubalus bubalis ) in a commercial dairy farm in Kerala, India. Parasitology 2016; 143(1): 69-74. http://dx.doi.org/10.1017/S0031182015001468. PMid:26522773.
http://dx.doi.org/10.1017/S003118201500...
), a previous study reported a Theileria sp. related to the T. buffeli /orientalis group that infects water buffaloes in the Brazilian Amazon region ( SILVEIRA et al., 2016 Silveira JAG, Oliveira CHS, Silvestre BT, Albernaz TT, Leite RC, Barbosa JD, et al. Molecular assays reveal the presence of Theileria spp. and Babesia spp. in Asian water buffaloes (Bubalus bubalis, Linnaeus, 1758) in the Amazon region of Brazil. Ticks Tick Borne Dis 2016; 7(5): 1017-1023. http://dx.doi.org/10.1016/j.ttbdis.2016.05.009. PMid:27344507.
http://dx.doi.org/10.1016/j.ttbdis.2016...
).

In Brazil, cattle and buffalo live and graze together and thus may share pathogens. A previous study of a multispecies grazing system found a single Anaplasma marginale strain that infects coexisting cattle, buffalo and ticks ( SILVA et al., 2014a Silva JB, Cabezas-Cruz A, Fonseca AH, Barbosa JD, Fuente J. Infection of water buffalo in Rio de Janeiro Brazil with Anaplasma marginale strains also reported in cattle. Vet Parasitol 2014a; 205(3-4): 730-734. http://dx.doi.org/10.1016/j.vetpar.2014.09.009. PMid:25260335.
http://dx.doi.org/10.1016/j.vetpar.2014...
). A. marginale is a tick-borne bacterium that causes bovine anaplasmosis ( DUMLER et al., 2001 Dumler JS, Barbet AF, Bekker CP, Dasch GA, Palmer GH, Ray SC, et al. Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and ‘HGE agent’ as subjective synonyms of Ehrlichia phagocytophila. Int J Syst Evol Microbiol 2001; 51(Pt 6): 2145-2165. http://dx.doi.org/10.1099/00207713-51-6-2145. PMid:11760958.
http://dx.doi.org/10.1099/00207713-51-6...
), and it is widely spread throughout Brazil ( POHL et al., 2013 Pohl AE, Cabezas-Cruz A, Ribeiro MF, Silveira JA, Silaghi C, Pfister K, et al. Detection of genetic diversity of Anaplasma marginale isolates in Minas Gerais, Brazil. Rev Bras Parasitol Vet 2013; 22(1): 129-135. http://dx.doi.org/10.1590/S1984-29612013000100024. PMid:24252959.
http://dx.doi.org/10.1590/S1984-2961201...
). However, data on A. marginale in buffaloes are scant ( SILVA et al., 2014c Silva JB, Vinhote WMS, Oliveira CMC, André MR, Machado RZ, Fonseca AH, et al. Molecular and serological prevalence of Anaplasma marginale in water buffaloes in northern Brazil. Ticks Tick Borne Dis 2014c; 5(2): 100-104. http://dx.doi.org/10.1016/j.ttbdis.2013.09.007. PMid:24246707.
http://dx.doi.org/10.1016/j.ttbdis.2013...
).

In Brazil, approximately 89,945 out of the one million water buffalo in the country are located in the state of Maranhão in the northeastern region of the country ( IBGE, 2017 Instituto Brasileiro de Geografia e Estatística – IBGE. Produção da pecuária municipal 2016 [online]. Rio de Janiero: IBGE; 2017 [cited 2017 December 30]. Available from: https://cidades.ibge.gov.br/brasil/ma/pesquisa/18/0?ano=2016
https://cidades.ibge.gov.br/brasil/ma/p...
). Buffalo farming has increased as an alternative use of land that is unfit for cattle breeding; furthermore, it has become an economically profitable option due to the ability of buffaloes to adapt to climate change and produce high-quality milk and meat ( BRASIL, 2007 Brasil. Vigilancia veterinária de doenças vesiculares: orientações gerais [online]. Brasília: Ministério da Agricultura, Pecuária e Abastecimento; 2007 [cited 2017 December 30]. Available from: http://www.agricultura.gov.br/assuntos/sanidade-animal-e-vegetal/saude-animal/arquivos-das-publicacoes-de-saude-animal/vigilancia-veterinaria.pdf/view
http://www.agricultura.gov.br/assuntos/...
). Although buffaloes have demonstrated a high adaptability, data on sanitation conditions is scarcely reported in the country ( BRASIL, 2007 Brasil. Vigilancia veterinária de doenças vesiculares: orientações gerais [online]. Brasília: Ministério da Agricultura, Pecuária e Abastecimento; 2007 [cited 2017 December 30]. Available from: http://www.agricultura.gov.br/assuntos/sanidade-animal-e-vegetal/saude-animal/arquivos-das-publicacoes-de-saude-animal/vigilancia-veterinaria.pdf/view
http://www.agricultura.gov.br/assuntos/...
). Thus, the aim of this study was to screen water buffaloes from the state of Maranhão for piroplasm and A. marginale occurrence using PCR assays.

A total of 287 water buffalo DNA samples were retrieved from a previous study ( SANTOS et al., 2018 Santos NJR, Brito DRB, Abate HL, Paixão SF, Soares EDS, Vieira TSWJ, et al. Hemotropic mycoplasmas infection in water buffaloes (Bubalus bubalis) from northeastern Brazil. Comp Immunol Microbiol Infect Dis 2018; 56(1): 27-29. http://dx.doi.org/10.1016/j.cimid.2017.12.003. PMid:29406279.
http://dx.doi.org/10.1016/j.cimid.2017....
). All samples were tested using a PCR for the housekeeping gene glyceraldehyde-3-phosphate dehydrogenase (GAPDH) to ensure successful DNA extraction, as previously described ( BIRKENHEUER et al., 2003 Birkenheuer AJ, Levy MG, Breitschwerdt EB. Development and evaluation of a seminested PCR for detection and differentiation of Babesia gibsoni (Asian genotype) and B. canis DNA in canine blood samples. J Clin Microbiol 2003; 41(9): 4172-4177. http://dx.doi.org/10.1128/JCM.41.9.4172-4177.2003. PMid:12958243.
http://dx.doi.org/10.1128/JCM.41.9.4172...
). DNA samples were screened by conventional PCR using a previously described primer set targeting the 18S rDNA gene of piroplasms ( ALMEIDA et al., 2012 Almeida AP, Marcili A, Leite RC, Nieri-Bastos FA, Domingues LN, Martins JR, et al. Coxiella symbiont in the tick Ornithodoros rostratus (Acari: Argasidae). Ticks Tick Borne Dis 2012; 3(4): 203-206. http://dx.doi.org/10.1016/j.ttbdis.2012.02.003. PMid:22480930.
http://dx.doi.org/10.1016/j.ttbdis.2012...
). A cattle-positive blood sample for B. bovis and ultrapure water were used as positive and negative controls, respectively. DNA samples were also screened by conventional PCR using a primer set targeting the A. marginale msp4 gene as described previously ( JOAZEIRO et al., 2015 Joazeiro AC, Martins J, Masuda A, Seixas A, Vaz IS. A PCR for differentiate between Anaplasma marginale and A. centrale. Acta Sci Vet 2015; 43(1): 1-7. ).

A fragment (356 bp) of the 18S rDNA gene from one piroplasm isolate was sequenced. The PCR product was purified from the agarose gel (PureLink®, Quick Gel Extraction Kit, Invitrogen, Carlsbad, CA, USA), evaluated by spectrophotometry for concentration and purity (Pico100 Picodrop® Spectrophotometer, Picodrop Limited, Hinxton, UK), and sequenced from both directions by Sanger method ( SANGER et al., 1977 Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 1977; 74(12): 5463-5467. http://dx.doi.org/10.1073/pnas.74.12.5463. PMid:271968.
http://dx.doi.org/10.1073/pnas.74.12.54...
) using a 3500 Genetic Analyzer (Applied Biosystems, Foster City, CA, USA). The assembled partial sequence of the 18S rDNA gene was compared with sequences deposited in the GenBank database using the basic local alignment search tool (BLASTn) ( ALTSCHUL et al., 1990 Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215(3): 403-410. http://dx.doi.org/10.1016/S0022-2836(05)80360-2. PMid:2231712.
http://dx.doi.org/10.1016/S0022-2836(05...
). The amplified nucleotide sequence of the Theileria sp. was submitted to GenBank (accession no. KY355137).

Theileria sp. 18S rDNA sequence was aligned using MAFFT 7 ( KATOH & STANDLEY, 2013 Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30(4): 772-780. http://dx.doi.org/10.1093/molbev/mst010. PMid:23329690.
http://dx.doi.org/10.1093/molbev/mst010...
) on Guidance2 ( SELA et al., 2015 Sela I, Ashkenazy H, Katoh K, Pupko T. GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Res. 2015;43(W1):W7-W14. http://dx.doi.org/10.1093/nar/gkv318. PMid:25883146.
http://dx.doi.org/10.1093/nar/gkv318 ...
). The best-fit evolutionary model was estimated as F81+I+G using jModeltest 2.1.4 ( DARRIBA et al., 2012 Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012; 9(8): 772. http://dx.doi.org/10.1038/nmeth.2109. PMid:22847109.
http://dx.doi.org/10.1038/nmeth.2109 ...
). The Bayesian Information Criterion (BIC) and Maximum Likelihood (ML) algorithms were used to the phylogenetic inference. Reconstruction was visualized with FigTree 1.4.0 software.

All water buffalo’s samples consistently amplified the GAPDH gene. One of the 287 (0.35%; 95% CI: 0.06 – 1.95) water buffalo tested was positive for Theileria sp. Sequencing of the 18S rDNA fragment (356 bp) showed that this gene region was ≥99% identical to multiple T. buffeli genes deposited in GenBank (EF126184, HQ840964, HM538205, HM538194, DQ104611). Phylogenetic 18S rDNA gene fragment analysis confirmed the close relationship of the water buffalo Theileria genotype of the present study with T. buffeli detected in India ( Figure 1 ). All samples were negative for A. marginale.

Figure 1
Phylogenetic tree based on partial sequences of the 18S rDNA gene, showing the relationship between the Theileria sp. detected in the water buffaloes ( Bubalus bubalis) from this study and other Theileria. Babesia bovis was used as an outgroup. The GenBank accession number is in parentheses after the species name and origin of each bacterium. Maximum Likelihood analyses were carried out applying the F81+I+G model and 1000 bootstrap replicates for all analyses.

In the present study, a Theileria sp. closely related to the T. buffeli /orientalis group was detected in water buffaloes from the state of Maranhão in northeastern Brazil. Theileira sp. was found in only one animal, supporting that this protozoan has a low prevalence in water buffaloes in Brazil ( SILVEIRA et al., 2016 Silveira JAG, Oliveira CHS, Silvestre BT, Albernaz TT, Leite RC, Barbosa JD, et al. Molecular assays reveal the presence of Theileria spp. and Babesia spp. in Asian water buffaloes (Bubalus bubalis, Linnaeus, 1758) in the Amazon region of Brazil. Ticks Tick Borne Dis 2016; 7(5): 1017-1023. http://dx.doi.org/10.1016/j.ttbdis.2016.05.009. PMid:27344507.
http://dx.doi.org/10.1016/j.ttbdis.2016...
). Haemaphysalis spp. ticks are the main vectors of species belonging to the T. buffeli/orientalis group ( UILENBERG et al., 1982 Uilenberg G, Perié NM, Lawrence JA, de Vos AJ, Paling RW, Spanjer AA. Causal agents of bovine theileriosis in southern Africa. Trop Anim Health Prod 1982; 14(3): 127-140. http://dx.doi.org/10.1007/BF02242143. PMid:6812250.
http://dx.doi.org/10.1007/BF02242143 ...
). In Brazil, despite Haemaphysalis juxtakochi (Cooley, 1946) ticks have been found infesting small red brocket deer (Mazama bororo Duarte) ( SZABÓ et al., 2006 Szabó MPJ, Labruna MB, Vogliotti A, Duarte JMB. Ticks (Acari: Ixodidae) on small red brocket deer (Mazama bororo Duarte) along deer trails in the Atlantic rain forest of southeastern Brazil. Syst Appl Acarol 2006; 11(1): 41-45. http://dx.doi.org/10.11158/saa.11.1.4.
http://dx.doi.org/10.11158/saa.11.1.4 ...
) and Brazilian dwarf brocket deer (Mazama nana) ( MARTINS et al., 2007 Martins JR, Salomão EL, Doyle RL, Onofrio V, Barros-Battesti DM, Guglielmone AA. Haemaphysalis juxtakochi Cooley, 1946 (Acari: Ixodidae) parasitando Mazama nana (Hensel, 1872) (Artiodactyla: Cervidae) no Estado do Rio Grande do Sul. Rev Bras Parasitol Vet 2007; 16(3): 171-173. http://dx.doi.org/10.1590/S1984-29612007000300012. PMid:18078606.
http://dx.doi.org/10.1590/S1984-2961200...
), this tick species has never been associated to buffaloes in the country. However, both tick species have never been associated as vectors of T. buffeli/orientalis , which may explain the low prevalence of infection found in this sample. Conversely, Rhipicephalus microplus ticks are endemic in Brazil ( DANTAS-TORRES et al., 2009 Dantas-Torres F, Onofrio VC, Barros-Battesti DM. The ticks (Acari: Ixodida: Argasidae, Ixodidae) of Brazil. Syst Appl Acarol 2009; 14(1): 30-46. http://dx.doi.org/10.11158/saa.14.1.4.
http://dx.doi.org/10.11158/saa.14.1.4 ...
), hampering livestock production and causing annual economic losses estimated at 3.24 billion USD ( GRISI et al., 2014 Grisi L, Leite RC, Martins JRS, Barros ATM, Andreotti R, Cançado PHD, et al. Reassessment of the potential economic impact of cattle parasites in Brazil. Rev Bras Parasitol Vet 2014; 23(2): 150-156. http://dx.doi.org/10.1590/S1984-29612014042. PMid:25054492.
http://dx.doi.org/10.1590/S1984-2961201...
). Additional studies are necessary to elucidate the putative tick vector of the Theileria sp. found in the present study.

Clinical signs of Theileria spp. infection in water buffaloes are still controversial ( SIVAKUMAR et al., 2014 Sivakumar T, Tattiyapong M, Fukushi S, Hayashida K, Kothalawala H, Silva SS, et al. Genetic characterization of Babesia and Theileria parasites in water buffaloes in Sri Lanka. Vet Parasitol 2014; 200(1-2): 24-30. http://dx.doi.org/10.1016/j.vetpar.2013.11.029. PMid:24365246.
http://dx.doi.org/10.1016/j.vetpar.2013...
), although fatal cases of theileriosis may occur during outbreaks ( VINODKUMAR et al., 2016 Vinodkumar K, Shyma V, Justin DK, Ashok S, Anu JP, Mini K, et al. Fatal Theileria orientalis N2 genotype infection among Asian water buffaloes (Bubalus bubalis ) in a commercial dairy farm in Kerala, India. Parasitology 2016; 143(1): 69-74. http://dx.doi.org/10.1017/S0031182015001468. PMid:26522773.
http://dx.doi.org/10.1017/S003118201500...
). In a previous study in water buffaloes from Brazil, Theileria infection was associated to lymphoproliferative disease ( SILVEIRA et al., 2016 Silveira JAG, Oliveira CHS, Silvestre BT, Albernaz TT, Leite RC, Barbosa JD, et al. Molecular assays reveal the presence of Theileria spp. and Babesia spp. in Asian water buffaloes (Bubalus bubalis, Linnaeus, 1758) in the Amazon region of Brazil. Ticks Tick Borne Dis 2016; 7(5): 1017-1023. http://dx.doi.org/10.1016/j.ttbdis.2016.05.009. PMid:27344507.
http://dx.doi.org/10.1016/j.ttbdis.2016...
). T. orientalis is distributed worldwide and is well known to cause clinical disease in cattle ( WATTS et al., 2016 Watts JG, Playford MC, Hickey KL. Theileria orientalis: a review. N Z Vet J 2016; 64(1): 3-9. http://dx.doi.org/10.1080/00480169.2015.1064792. PMid:26143684.
http://dx.doi.org/10.1080/00480169.2015...
). Considering that multispecies grazing is a common practice in this region of Brazil, further studies are needed to evaluate cattle from the same Brazilian region, as cross-species transmission may occur and may lead to important economic consequences for the cattle industry.

Anaplasma marginale is endemic in Brazilian cattle herds ( JOAZEIRO et al., 2015 Joazeiro AC, Martins J, Masuda A, Seixas A, Vaz IS. A PCR for differentiate between Anaplasma marginale and A. centrale. Acta Sci Vet 2015; 43(1): 1-7. ; KOCAN et al., 2010 Kocan KM, Fuente J, Blouin EF, Coetzee JF, Ewing SA. The natural history of Anaplasma marginale. Vet Parasitol 2010; 167(2-4): 95-107. http://dx.doi.org/10.1016/j.vetpar.2009.09.012. PMid:19811876.
http://dx.doi.org/10.1016/j.vetpar.2009...
). Although studies on A. marginale in water buffaloes are scarce in Brazil ( SILVA et al., 2014a Silva JB, Cabezas-Cruz A, Fonseca AH, Barbosa JD, Fuente J. Infection of water buffalo in Rio de Janeiro Brazil with Anaplasma marginale strains also reported in cattle. Vet Parasitol 2014a; 205(3-4): 730-734. http://dx.doi.org/10.1016/j.vetpar.2014.09.009. PMid:25260335.
http://dx.doi.org/10.1016/j.vetpar.2014...
, b Silva JB, Fonseca AH, Barbosa JD, Cabezas-Cruz A, Fuente J. Low genetic diversity associated with low prevalence of Anaplasma marginale in water buffaloes in Marajó Island, Brazil. Ticks Tick Borne Dis 2014b; 5(6): 801-804. http://dx.doi.org/10.1016/j.ttbdis.2014.06.003. PMid:25108778.
http://dx.doi.org/10.1016/j.ttbdis.2014...
, c Silva JB, Vinhote WMS, Oliveira CMC, André MR, Machado RZ, Fonseca AH, et al. Molecular and serological prevalence of Anaplasma marginale in water buffaloes in northern Brazil. Ticks Tick Borne Dis 2014c; 5(2): 100-104. http://dx.doi.org/10.1016/j.ttbdis.2013.09.007. PMid:24246707.
http://dx.doi.org/10.1016/j.ttbdis.2013...
), previous studies have detected the same strains of A. marginale in water buffaloes and cattle ( SILVA et al., 2014a Silva JB, Cabezas-Cruz A, Fonseca AH, Barbosa JD, Fuente J. Infection of water buffalo in Rio de Janeiro Brazil with Anaplasma marginale strains also reported in cattle. Vet Parasitol 2014a; 205(3-4): 730-734. http://dx.doi.org/10.1016/j.vetpar.2014.09.009. PMid:25260335.
http://dx.doi.org/10.1016/j.vetpar.2014...
). Thus, co-grazing of cattle and water buffaloes may be an important risk factor for A. marginale infection, and this hypothesis should be further evaluated.

Our results reinforce that Theileira sp. is closely related to the T. buffeli/orientalis group occurs in water buffaloes’ samples from Brazil. Future studies are needed investigating clinical signs of infection and the main vector for disease transmission in this country.

Acknowledgements

This study is part of a Master’s degree for Hugo Abate at the Universidade Estadual de Londrina. Dr. Abate was sponsored by a fellowship from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação Araucária at the time of the study.

References

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Publication Dates

  • Publication in this collection
    08 Nov 2018
  • Date of issue
    Oct-Dec 2018

History

  • Received
    20 Mar 2018
  • Accepted
    07 Aug 2018
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
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