Experimental and Applied Acarology

, Volume 73, Issue 1, pp 91–102 | Cite as

Molecular detection of pathogens in ticks infesting cattle in Nampula province, Mozambique

  • Ana Marcília Matsimbe
  • Vlademiro Magaia
  • Gustavo Seron Sanches
  • Luís Neves
  • Emília Noormahomed
  • Sandra Antunes
  • Ana Domingos
Article
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Abstract

Ticks are ectoparasites that can act as vectors of a large number of pathogens in wild and domestic animals, pets, and occasionally humans. The global threat of emerging or re-emerging tick-borne diseases supports the need for research focused in the zoonotic transmission, especially in countries like Mozambique where rural populations are in close contact with domestic animals. The present study aims to: (1) identify tick species infesting cattle from Monapo and Nacala Porto, districts of Nampula province, Mozambique; and (2) investigate the presence of pathogens in the collected ticks. A total of 646 ticks were collected from cattle and morphologically identified as Amblyomma variegatum, Rhipicephalus microplus, and R. evertsi evertsi. For convenience, 72 A. variegatum and 15 R. microplus from Monapo, and 30 A. variegatum from Nacala Porto were screened for the presence of the selected pathogens: Rickettsia spp. (A. variegatum), and Babesia/Theileria spp. and Anaplasma/Ehrlichia spp. (R. microplus). Rickettsia africae was detected in four of the 72 A. variegatum collected in Monapo (5.6%). Additionally, one R. microplus tick (6.7%) was positive for Theileria velifera, one positive for Colpodella spp., one positive for Candidatus Midichloria mitochondrii, and another one positive for Anaplasma ovis. Using the present approach, no microorganisms were detected in tick samples from Nacala Porto. These findings expand our knowledge about the repertoire of tick-borne microorganisms in ticks in Nampula province, Mozambique.

Keywords

Mozambique Cattle ticks Zoonotic pathogens PCR 
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Notes

Acknowledgements

This manuscript is a part of the dissertation that Ana Marcília Matsimbe developed under the master course on Tropical Medicine and Global Health funded by the Medical Education partnership Initiative grants number R24TW008908 from the Fogarty International Center, National Institutes of Health (NIH). The authors acknowledge Varda Shkap (Kimron Veterinary Institute, Israel) for kindly providing B. bigemina control and Rosangela Zacarias Machado (Universidade Estadual Paulista-Campus Jaboticabal, Brazil) for the E. canis control. We also thank Professor Virgílio do Rosário for valuable advices. FCT for funds to GHTM—UID/Multi/04413/2013.

Author contributions

AM and VM participated in tick collections, tick identification, conducted DNA extraction and performed R. africae PCR screening. GS and SA performed the PCR for Babesia/Theileria and Anaplasmataceae family. GS, SA, and AD analysed data and wrote the article. LN, EM and AD designed and supervised the study. All authors edited and approved the final manuscript.

References

  1. Althaus F, Greub G, Raoult D, Genton B (2010) African tick-bite fever: a new entity in the differential diagnosis of multiple eschars in travellers. Description of five cases imported from South Africa to Switzerland. Int J Infect Dis 14:e274–e276. doi: 10.1016/j.ijid.2009.11.021 CrossRefPubMedGoogle Scholar
  2. Armstrong PM, Katavolos P, Caporale DA et al (1998) Diversity of Babesia infecting deer ticks (Ixodes dammini). Am J Trop Med Hyg 58:739–742CrossRefPubMedGoogle Scholar
  3. Baneth G (2014) Tick-borne infections of animals and humans: a common ground. Inter J Parasitol 44:591–596. doi: 10.1016/j.ijpara.2014.03.011 CrossRefGoogle Scholar
  4. Bell-Sakyi L, Koney EBM, Dogbey O, Walker AR (2004) Incidence and prevalence of tick-borne haemoparasites in domestic ruminants in Ghana. Vet Parasitol 124:25–42. doi: 10.1016/j.vetpar.2004.05.027 CrossRefPubMedGoogle Scholar
  5. Beninati T, Lo N, Sacchi L, Genchi C, Noda H, Bandi C (2004) A novel alpha-proteobacterium resides in the mitochondria of ovarian cells of the tick Ixodes ricinus. Appl Environ Microbiol 70:2596–2602. doi: 10.1128/AEM.70.5.2596-2602.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bock R, Jackson L, De Vos A, Jorgensen W (2004) Babesiosis of cattle. Parasitology 129:S247–S269. doi: 10.1017/S0031182004005190 CrossRefPubMedGoogle Scholar
  7. Bournez L, Cangi N, Lancelot R et al (2015) Parapatric distribution and sexual competition between two tick species, Amblyomma variegatum and A. hebraeum (Acari, Ixodidae), in Mozambique. Parasit Vectors 8:504. doi: 10.1186/s13071-015-1116-7 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Capinera JL (2008) Encyclopedia of entomology. Springer, New YorkCrossRefGoogle Scholar
  9. Chochlakis D, Ioannou I, Tselentis Y, Psaroulaki A (2010) Human anaplasmosis and Anaplasma ovis variant. Emerg Infect Dis 16:1031–1032. doi: 10.3201/eid1606.090175 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cong L, Yuan CL, Keeling PJ, Krause PJ, Horak A, Bent S, Rollend L et al (2012) Colpodella spp.–like parasite infection in woman, China. Emerg Infect Dis 18:125–127. doi: 10.3201/eid1801.110716 CrossRefGoogle Scholar
  11. de la Fuente J, Estrada-Peña A, Venzal JM, Kocan KM, Sonenshine DE (2008) Overview: ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci 13:6938–6946. doi: 10.2741/3200 CrossRefPubMedGoogle Scholar
  12. De Matos C, Sitoe C, Neves L, Nöthling JO, Horak IG (2009) The comparative prevalence of five ixodid tick species infesting cattle and goats in Maputo Province, Mozambique. Onderstepoort J Vet Res 76:201–208. doi: 10.4102/ojvr.v76i2.45 CrossRefPubMedGoogle Scholar
  13. Delord M, Socolovschi C, Parola P (2014) Rickettsioses and Q fever in travelers (2004–2013). Travel Med Infect Dis 12:443–458. doi: 10.1016/j.tmaid.2014.08.006 CrossRefPubMedGoogle Scholar
  14. Dennis DT, Piesman JF (2005) Overview of tick-borne infections of humans. In: Goodman JL, Dennis DT, Sonenshine DE (eds) Tick-borne diseases of humans, 1st edn. American Society for Microbiology, Washington, pp 3–11CrossRefGoogle Scholar
  15. Dergousoff SJ, Chilton NB (2011) Novel genotypes of Anaplasma bovis, Candidatus Midichloria sp. and Ignatzschineria sp. in the Rocky Mountain wood tick, Dermacentor andersoni. Vet Microbiol 150:100–106. doi: 10.1016/j.vetmic.2011.01.018 CrossRefPubMedGoogle Scholar
  16. Di Venere M, Fumagalli M, Cafiso A, De Marco L et al (2015) Ixodes ricinus and its endosymbiont Midichloria mitochondrii: a comparative proteomic analysis of salivary glands and ovaries. PLoS ONE 10(9):e0138842. doi: 10.1371/journal.pone.0138842 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Domingos A, Antunes S, Borges L, do Rosário VE (2013) Approaches towards tick and tick-borne diseases control. Rev Soc Bras Med Trop 46:265–269. doi: 10.1590/0037-8682-0014-2012 CrossRefPubMedGoogle Scholar
  18. Eisler MC, Magona JW, Jonsson NN, Revie CW (2007) A low cost decision support tool for the diagnosis of endemic bovine infectious diseases in the mixed crop–livestock production system of sub-Saharan Africa. Epidemiol Infect 135:67–75. doi: 10.1017/S0950268806006571 CrossRefPubMedGoogle Scholar
  19. Elelu N, Ferrolho J, Couto J, Domingos A, Eisler MC (2016) Molecular diagnosis of the tick-borne pathogen Anaplasma marginale in cattle blood samples from Nigeria using qPCR. Exp Appl Acarol 70:501–510CrossRefPubMedGoogle Scholar
  20. Epis S, Sassera D, Beninati T, Lo N, Beati L et al (2008) Midichloria mitochondrii is widespread in hard ticks (Ixodidae) and resides in the mitochondria of phylogenetically diverse species. Parasitology 135:485–494. doi: 10.1017/S0031182007004052 CrossRefPubMedGoogle Scholar
  21. Estrada-Peña A, Jongejan F (1999) Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp Appl Acarol 23:685–715CrossRefPubMedGoogle Scholar
  22. Ferrolho J, Antunes S, Santos AS, Velez R, Padre L, Cabezas-Cruz A, Santos-Silva MM, Domingos A (2016) Detection and phylogenetic characterization of Theileria spp. and Anaplasma marginale in Rhipicephalus bursa in Portugal. Ticks Tick Borne Dis 7:443–448. doi: 10.1016/j.ttbdis.2016.01.004 CrossRefPubMedGoogle Scholar
  23. Fournier PE, Roux V, Raoult D (1998) Phylogenetic analysis of spotted fever group rickettsiae by study of the outer surface protein rOmpA. Int J Syst Bacteriol 48:839–849CrossRefPubMedGoogle Scholar
  24. Friedhoff KT (1997) Tick-borne diseases of sheep and goats caused by Babesia, Theileria or Anaplasma spp. Parassitologia 39:99–109PubMedGoogle Scholar
  25. Grisi L, Leite RC, Martins JRS, Barros ATM, Andreotti R, Cancado PHD, Perez de Leon AA, Pereira JB, Villela HS (2014) Reassessment of the potential economic impact of cattle parasites in Brazil. Braz J Vet Parasitol 23:150–156. doi: 10.1590/S1984-29612014042 CrossRefGoogle Scholar
  26. Guglielmone AA, Mangold AJ, Viñabal AE (1991) Ticks (Ixodidae) parasitizing humans in four provinces of north-western Argentina. Ann Trop Med Parasitol 85:539–542CrossRefPubMedGoogle Scholar
  27. Horak IG, Nyangiwe N, De Matos C, Neves L (2009) Species composition and geographic distribution of ticks infesting cattle, goats and dogs in a temperate and in a subtropical region of south-east Africa. Onderstepoort J Vet Res 76:263–276PubMedGoogle Scholar
  28. Hornok S, Elek V, de la Fuente J, Naranjo V et al (2007) First serological and molecular evidence on the endemicity of Anaplasma ovis and A. marginale in Hungary. Vet Microbiol 122:316–322. doi: 10.1016/j.vetmic.2007.01.024 CrossRefPubMedGoogle Scholar
  29. Jensenius M, Fournier PE, Kelly P, Myrvang B, Raoult D (2003) African tick bite fever. Lancet Infect Dis 3:557–564. doi: 10.1016/S1473-3099(03)00739-4 CrossRefPubMedGoogle Scholar
  30. Jensenius M, Davis X, von Sonnenburg F, Schwartz E et al (2009) Multicenter GeoSentinel analysis of rickettsial diseases in international travelers, 1996–2008. Emerg Infect Dis 15:1791–1798. doi: 10.3201/eid1511.090677 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Jongejan F, Uilenberg G (2004) The global importance of ticks. Parasitology 129:S3–S14. doi: 10.1017/S0031182004005967 CrossRefPubMedGoogle Scholar
  32. Jonsson NN (2006) The productivity effects of cattle tick (Boophilus microplus) infestation on cattle, with particular reference to Bos indicus cattle and their crosses. Vet Parasitol 137:1–10. doi: 10.1016/j.vetpar.2006.01.010 CrossRefPubMedGoogle Scholar
  33. Kelly PJ, Beati L, Mason PR, Matthewman LA et al (1996) Rickettsia africae sp nov, the etiological agent of African tick bite fever. Int J Syst Bacteriol 46:611–614CrossRefPubMedGoogle Scholar
  34. Kocan KM, de la Fuente J, Blouin EF, Garcia-Garcia JC (2004) Anaplasma marginale (Rickettsiales: Anaplasmataceae): recent advances in defining host-pathogen adaptations of a tick-borne rickettsia. Parasitology 129:S285–S300. doi: 10.1017/S0031182003004700 CrossRefPubMedGoogle Scholar
  35. Kubelová M, Mazancová J, Siroký P (2012) Theileria, Babesia, and Anaplasma detected by PCR in ruminant herds at Bié Province, Angola. Parasite 19:417–422. doi: 10.1051/parasite/2012194417 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Labruna MB, Whitworth T, Horta MC, Bouyer DH et al (2004) Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of São Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol 42:90–98. doi: 10.1128/JCM.42.1.90-98.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Lamattina D, Nava S (2016) Ticks infesting humans in Northern Misiones, Argentina. Medicina 76:89–92. doi: 10.1016/j.ttbdis.2013.10.005 PubMedGoogle Scholar
  38. Leander BS, Keeling PJ (2003) Morphostasis in alveolate evolution. Trends Ecol Evol 18:395–402. doi: 10.1016/S0169-5347(03)00152-6 CrossRefGoogle Scholar
  39. Liyanaarachchi DR, Rajakaruna RS, Dikkumbura AW, Rajapakse RP (2015) Ticks infesting wild and domestic animals and humans of Sri Lanka with new host records. Acta Trop 142:64–70. doi: 10.1016/j.actatropica.2014.11.001 CrossRefPubMedGoogle Scholar
  40. Lo N, Beninati T, Sassera D, Bouman EA, Santagati S, Gern L et al (2006) Widespread distribution and high prevalence of an alpha-proteobacterial symbiont in the tick Ixodes ricinus. Environ Microbiol 8:1280–1287. doi: 10.1111/j.1462-2920.2006.01024.x CrossRefPubMedGoogle Scholar
  41. Lorusso V, Gruszka KA, Majekodunmi A, Igweh A, Welburn SC, Picozzi K (2013) Rickettsia africae in Amblyomma variegatum ticks, Uganda and Nigeria. Emerg Infect Dis 19:1705–1707. doi: 10.3201/eid1910.130389 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Lorusso V, Wijnveld M, Majekodunmi AO, Dongkum C et al (2016) Tick-borne pathogens of zoonotic and veterinary importance in Nigerian cattle. Parasit Vectors 9:217. doi: 10.1186/s13071-016-1504-7 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Martins TM, Pedro OC, Caldeira RA, do Rosário VE, Neves L, Domingos A (2008) Detection of bovine babesiosis in Mozambique by a novel seminested hot-start PCR method. Vet Parasitol 153:225–230. doi: 10.1016/j.vetpar.2008.01.037 CrossRefPubMedGoogle Scholar
  44. Martins TM, Neves L, Pedro OC, Fafetine JM, do Rosário VE, Domingos A (2010) Molecular detection of Babesia spp. and other haemoparasitic infections of cattle in Maputo Province, Mozambique. Parasitology 137:1–8CrossRefGoogle Scholar
  45. Mediannikov O, Fenollar F (2014) Looking in ticks for human bacterial pathogens. Microb Pathog 77:142–148. doi: 10.1016/j.micpath.2014.09.008 CrossRefPubMedGoogle Scholar
  46. Mediannikov O, Trape JF, Diatta G, Parola P et al (2010) Rickettsia africae, Western Africa. Emerg Infect Dis 16:571–573. doi: 10.3201/eid1603.090346 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Molyneux D, Hallaj Z, Keusch GT et al (2011) Zoonoses and marginalised infectious diseases of poverty: where do we stand? Parasit Vectors 4:106. doi: 10.1186/1756-3305-4-106 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Ndip LM, Fokam EB, Bouyer DH et al (2004) Detection of Rickettsia africae in patients and ticks along the coastal region of Cameroon. Am J Trop Med Hyg 71:363–366. doi: 10.1089/vbz.2012.0977 PubMedGoogle Scholar
  49. Oostvogel PM, van Doornum GJ, Ferreira R, Vink J et al (2007) African tick-bite fever in travelers, Swaziland. Emerg Infect Dis 13:353–355. doi: 10.3201/eid1111.050852 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Otranto D, Dantas-Torres F, Giannelli A, Latrofa MS, Cascio A, Cazzin S (2014) Ticks infesting humans in Italy and associated pathogens. Parasit Vectors 7:328. doi: 10.1186/1756-3305-7-328 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Parola P, Roux V, Camicas JL et al (2000) Detection of Ehrlichiae in African ticks by polymerase chain reaction. Trans R Soc Trop Med Hyg 94:707–708. doi: 10.1016/S0035-9203(00)90243-8 CrossRefPubMedGoogle Scholar
  52. Parola P, Inokuma H, Camica JL, Brouqui P et al (2001) Detection and identification of spotted fever group rickettsiae and Ehrlichiae in African ticks. Emerg Infect Dis 7:1014–1017. doi: 10.3201/eid0706.010616 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Parola P, Paddock CD, Socolovschi C, Labruna MB et al (2013) Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev 26:657–702. doi: 10.1128/CMR.00032-13 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Ramos VN, Osava CF, Piovezan U, Szabó MP (2014) Complementary data on four methods for sampling free-living ticks in the Brazilian Pantanal. Braz J Vet Parasitol 23:516–521. doi: 10.1590/S1984-29612014091 CrossRefGoogle Scholar
  55. Roch N, Epaulard O, Pelloux I, Pavese P et al (2008) African tick bite fever in elderly patients: 8 cases in French tourists returning from South Africa. Clin Infect Dis 47:e28–e35. doi: 10.1086/589868 CrossRefPubMedGoogle Scholar
  56. Rocha A, Starkey P, Dionisio AC (1991) Cattle production and utilisation in smallholder farming systems in Southern Mozambique. Agric Syst 1:55–75CrossRefGoogle Scholar
  57. Santos Dias JAT (1993) Some data concerning the ticks (Acarina-Ixodoida) presently known in Mozambique. Garcia de Orta Ser Zool 18:27–48Google Scholar
  58. Socolovschi C, Huynh TP, Davoust B, Gomez J, Raoult D, Parola P (2009) Transovarial and trans-stadial transmission of Rickettsiae africae in Amblyomma variegatum ticks. Clin Microbiol Infect 15:317–318. doi: 10.1111/j.1469-0691.2008.02278.x CrossRefPubMedGoogle Scholar
  59. Suarez C, Noah S (2011) Emerging perspectives in the research of bovine babesiosis and anaplasmosis. Vet Parasitol 180:109–125. doi: 10.1016/j.vetpar.2011.05.032 CrossRefPubMedGoogle Scholar
  60. Venzal JM, Estrada-Pena A, Portillo A, Mangold AJ et al (2012) Rickettsia parkeri: a Rickettsial pathogen transmitted by ticks in endemic areas for spotted fever rickettsiosis in southern Uruguay. Rev Inst Med Trop 54:131–134. doi: 10.1590/S0036-46652012000300003 CrossRefGoogle Scholar
  61. Walker AR, Bouattour A, Camicas JL, Estrada-Pena A et al (2003) Ticks of domestic animals in Africa: a guide to identification of species. Bioscience Reports, EdinburghGoogle Scholar
  62. Wernecke M, Schein E, Voigt WP, Uilenberg G (1979) On the life cycle of Theileria velifera (Uilenberg, 1964) in the gut and the haemolymph of the tick vector Amblyomma variegatum (Fabriciu, 1794). Tropenmed Parasitol 30:318–322Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Centro de Estudos de Pós-Graduação e ExtensãoUniversidade LúrioNampulaMozambique
  2. 2.Centro de BiotecnologiaUniversidade Eduardo MondlaneMaputoMozambique
  3. 3.Global Health and Tropical Medicine, Instituto de Higiene e Medicina TropicalUniversidade Nova de LisboaLisbonPortugal
  4. 4.Department of Veterinary Tropical DiseasesUniversity of PretoriaOnderstepoortSouth Africa
  5. 5.Department of Microbiology, Faculty of MedicineUniversidade Eduardo MondlaneMaputoMozambique
  6. 6.Department of Medicine, Infectious Disease DivisionUniversity of CaliforniaSan DiegoUSA
  7. 7.Mozambique Institute for Health Education and Research (MIHER)MaputoMozambique

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