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Detection of lumpy skin disease virus in saliva of ticks fed on lumpy skin disease virus-infected cattle

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Abstract

Lumpy skin disease is an economically important disease of cattle that is caused by the lumpy skin disease virus (LSDV), which belongs to the genus Capripoxvirus. It is endemic in Africa and outbreaks have also been reported in the Middle-East. Transmission has mostly been associated with blood-feeding insects but recently, the authors have demonstrated mechanical transmission by Rhipicephalus appendiculatus as well as mechanical/intrastadial and transstadial transmission by Amblyomma hebraeum. Saliva is the medium of transmission of pathogens transmitted by biting arthropods and, simultaneously, it potentiates infection in the vertebrate host. This study aimed to detect LSDV in saliva of A. hebraeum and R. appendiculatus adult ticks fed, as nymphs or as adults, on LSDV-infected animals, thereby also demonstrating transstadial or mechanical/intrastadial passage of the virus in these ticks. Saliva samples were tested for LSDV by real-time PCR and virus isolation. Supernatants obtained from virus isolation were further tested by real-time PCR to confirm that the cytopathic effects observed were due to LSDV. Lumpy skin disease virus was detected, for the first time, in saliva samples of both A. hebraeum and R. appendiculatus ticks. At the same time, mechanical/intrastadial and transstadial passage of the virus was demonstrated and confirmed in R. appendiculatus and A. hebraeum.

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References

  • Balashov YS (1967) Blood-sucking ticks (Ixodoidea)-vectors of diseases of man and animals.; Krovososushchie kleshchi (Ixodoidea)-perenoschiki boleznei chel-oveka i zhivotnykh

  • Booth TF, Davies CR, Jones LD, Staunton D, Nuttall PA (1989) Anatomical basis of Thogoto virus infection in BHK cell culture and in the Ixodid tick vector, Rhipicephalus appendiculatus. J Gen Virol 70:1093–1104

    Article  PubMed  Google Scholar 

  • Bowden TR, Babiuk SL, Parkyn GR, Copps JS, Boyle DB (2008) Capripoxvirus tissue tropism and shedding: a quantitative study in experimentally infected sheep and goats. Virology 371:380–393

    Article  PubMed  CAS  Google Scholar 

  • Bremer WG, Schaefer JJ, Wagner ER, Ewing SA, Rikihisa Y, Needham GR, Jittapalapong S, Moore DL, Stich RW (2005) Transstadial and intrastadial experimental transmission of Ehrlichia canis by male Rhipicephalus sanguineus. Vet Parasitol 131:95–105

    Article  PubMed  Google Scholar 

  • Brown SJ (1988) Evidence for regurgitation by Amblyomma americanum. Vet Parasitol 28:335–342

    Article  PubMed  CAS  Google Scholar 

  • Carn VM, Kitching RP (1995) An investigation of possible routes of transmission of lumpy skin disease virus (neethling). Epidemiol Infect 114:219–226

    Article  PubMed  CAS  Google Scholar 

  • Chalaire KC, Kim TK, Garcia-Rodriguez H, Mulenga A (2011) Amblyomma americanum (L.) (Acari: Ixodidae) tick salivary gland serine protease inhibitor (serpin) 6 is secreted into tick saliva during tick feeding. J Exp Biol 214:665–673

    Article  PubMed  CAS  Google Scholar 

  • Chihota CM, Rennie LF, Kitching RP, Mellor PS (2001) Mechanical transmission of lumpy skin disease virus by Aedes aegypti (Diptera: Culicidae). Epidemiol Infect 126:317–321

    Article  PubMed  CAS  Google Scholar 

  • Chihota CM, Rennie LF, Kitching RP, Mellor PS (2003) Attempted mechanical transmission of lumpy skin disease virus by biting insects. Med Vet Entomol 17:294–300

    Article  PubMed  CAS  Google Scholar 

  • Connat JL (1991) Demonstration of regurgitation of gut content during blood meals of the tick Ornithodoros moubata. Possible role in the transmission of pathogenic agents. Parasitol Res 77:452–454

    Article  PubMed  CAS  Google Scholar 

  • Cowdry EV, Ham AW (1932) Studies on east coast fever. I. The life cycle of the parasite in ticks. Parasitology 24:1–49

    Article  Google Scholar 

  • Cupp EW (1991) Biology of ticks. Vet Clin North Am Small Anim Pract 21:1–26

    PubMed  CAS  Google Scholar 

  • Gilbert L, Jones LD, Hudson PJ, Gould EA, Reid HW (2000) Role of small mammals in the persistence of Louping-ill virus: field survey and tick co-feeding studies. Med Vet Entomol 14:277–282

    Article  PubMed  CAS  Google Scholar 

  • Gill HS, Walker AR (1987) The salivary glands of Hyalomma anatolicum anatolicum: structural changes during attachment and feeding. Int J Parasitol 17:1381–1392

    Article  PubMed  CAS  Google Scholar 

  • Gill HS, Walker AR (1988) The salivary glands of Hyalomma anatolicum anatolicum: nature of salivary gland components and their role in tick attachment and feeding. Int J Parasitol 18:83–93

    Article  PubMed  CAS  Google Scholar 

  • Jones LD, Hodgson E, Nuttall PA (1989) Enhancement of virus transmission by tick salivary glands. J Gen Virol 70:1895–1898

    Article  PubMed  Google Scholar 

  • Jones LD, Hodgson E, Williams T, Higgs S, Nuttall PA (1992a) Saliva activated transmission (SAT) of Thogoto virus: relationship with vector potential of different haematophagous arthropods. Med Vet Entomol 6:261–265

    Article  PubMed  CAS  Google Scholar 

  • Jones LD, Kaufman WR, Nuttall PA (1992b) Modification of the skin feeding site by tick saliva mediates virus transmission. Experientia 48:779–782

    Article  PubMed  CAS  Google Scholar 

  • Jones LD, Matthewson M, Nuttall PA (1992c) Saliva-activated transmission (SAT) of Thogoto virus: dynamics of SAT factor activity in the salivary glands of Rhipicephalus appendiculatus, Amblyomma variegatum and Boophilus microplus ticks. Exp Appl Acarol 13:241–248

    Article  PubMed  CAS  Google Scholar 

  • Jones LD, Gaunt M, Hails RS, Laurenson K, Hudson PJ, Reid H, Henbest P, Gould EA (1997) Transmission of louping ill virus between infected and uninfected ticks co-feeding on mountain hares. Med Vet Entomol 11:172–176

    Article  PubMed  CAS  Google Scholar 

  • Kaufman WR, Nuttall PA (1996) Amblyomma variegatum (Acari: Ixodidae): mechanism and control of arbovirus secretion in tick saliva. Exp Parasitol 82:316–323

    Article  PubMed  CAS  Google Scholar 

  • Kaufman WR, Nuttall PA (2003) Rhipicephalus appendiculatus (Acari: Ixodidae): dynamics of Thogoto virus infection in female ticks during feeding on guinea pigs. Exp Parasitol 104:20–25

    Article  PubMed  Google Scholar 

  • Kaufman WR, Bowman AS, Nuttall PA (2001) Salivary fluid secretion in the ixodid tick Rhipicephalus appendiculatus is inhibited by Thogoto virus infection. Exp Appl Acarol 25:661–674

    Article  PubMed  CAS  Google Scholar 

  • Kocan KM, Bezuidenhout JD (1987) Morphology and development of Cowdria ruminantium in Amblyomma ticks. Onderstepoort J Vet Res 54:177–182

    PubMed  CAS  Google Scholar 

  • Kocan KM, Stiller D (1992) Development of Anaplasma ovis (Rickettsiales: Anaplasmataceae) in male Dermacentor andersoni (Acari: Ixodidae) transferred from infected to susceptible sheep. J Med Entomol 29:98–107

    PubMed  CAS  Google Scholar 

  • Kocan KM, Bezuidenhout JD, Hart A (1987) Ultrastructural features of Cowdria ruminantium in midgut epithelial cells and salivary glands of nymphal Amblyomma hebraeum. Onderstepoort J Vet Res 54:87–92

    PubMed  CAS  Google Scholar 

  • Mans BJ, Neitz AWH (2004) Adaptation of ticks to a blood-feeding environment: evolution from a functional perspective. Insect Biochem Mol Biol 34:1–17

    Article  PubMed  CAS  Google Scholar 

  • Martin HM, Barnett SF, Vidler BO (1964) Cyclic development and longevity of Theileria parva in the tick Rhipicephalus appendiculatus. Exp Parasitol 15:527–555

    Article  PubMed  CAS  Google Scholar 

  • Norval RAI, Andrew HR, Yunker CE (1989) Pheromone-mediation of host-selection in bont ticks (Amblyomma hebraeum Koch). Science (Wash) 243:364–365

    Article  CAS  Google Scholar 

  • Norval RAI, Peter T, Sonenshine DE, Burridge MJ (1992) Responses of the ticks Amblyomma hebraeum and A. variegatum to known or potential components of the aggregation-attachment pheromone III Aggregation. Exp Appl Acarol 16:237–245

    Article  PubMed  CAS  Google Scholar 

  • Plowright W, Ferris RD (1958) The growth and cytopathogenicity of sheep-pox virus in tissue cultures. Brit J Exper Path 39:424–435

    CAS  Google Scholar 

  • Plowright W, Witcomb MA (1959) The growth in tissue cultures of a virus derived from lumpy-skin disease of cattle. J Pathol Bacteriol 78:397–407

    Article  PubMed  CAS  Google Scholar 

  • Ribeiro JMC, Zeidner NS, Ledin K, Dolan MC, Mather TN (2004) How much pilocarpine contaminates pilocarpine-induced tick saliva? Med Vet Entomol 18:20–24

    Article  PubMed  CAS  Google Scholar 

  • Sonenshine DE (1991) Biology of ticks. Oxford University Press, Oxford

    Google Scholar 

  • Stachurski F (2006) Attachment kinetics of the adult tick Amblyomma variegatum to cattle. Med Vet Entomol 20:317–324

    Article  PubMed  CAS  Google Scholar 

  • Titus RG, Ribeiro JMC (1990) The role of vector saliva in transmission of arthropod-borne disease. Parasitol Today 6:157–160

    Article  PubMed  CAS  Google Scholar 

  • Tuppurainen ES, Venter EH, Coetzer JA (2005) The detection of lumpy skin disease virus in samples of experimentally infected cattle using different diagnostic techniques. Onderstepoort J Vet Res 72:153–164

    Article  PubMed  CAS  Google Scholar 

  • Tuppurainen ESM, Stoltsz WH, Troskie M, Wallace DB, Oura CAL, Mellor PS, Coetzer JAW, Venter EH (2011) A potential role for ixodid (hard) tick vectors in the transmission of lumpy skin disease virus in cattle. Transbound Emerg Dis 58:93–104

    Article  Google Scholar 

  • Tuppurainen ESM, Lubinga JC, Stoltsz WH, Troskie M, Carpenter ST, Coetzer JAW, Venter EH, Oura CAL (2013) Mechanical transmission of lumpy skin disease virus by Rhipicephalus appendiculatus male ticks. Epidemiol Infect 141:425–430

    Article  Google Scholar 

  • Von Backstrom U (1945) Ngamiland cattle disease. Preliminary report on a new disease, the etiological agent being probably of an infectious nature. J S Afr Vet Med Assoc 16:29–35

    Google Scholar 

  • Walker JB (1970) Notes on the common tick species of East Africa. McDougall and Robertson, Cooper

    Google Scholar 

  • Walker A (2003) Ticks of domestic animals in Africa: a guide to identification of species. Bioscience Reports, Edinburgh

    Google Scholar 

  • Wang H, Nuttall PA (2001) Intra-stadial tick-borne Thogoto virus (Orthomyxoviridae) transmission: accelerated arbovirus transmission triggered by host death. Parasitology 122:439–446

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Henbest PJ, Nuttall PA (1999) Successful interrupted feeding of adult Rhipicephalus appendiculatus (Ixodidae) is accompanied by reprogramming of salivary gland protein expression. Parasitology 119:143–149

    Article  PubMed  CAS  Google Scholar 

  • Weiss KE (1968) Lumpy skin disease virus. Virol Monogr 3:111–131

    Google Scholar 

  • Wikel SK (1984) Immunomodulation of host responses to ectoparasite infestation—an overview. Vet Parasitol 14:321–339

    Article  PubMed  CAS  Google Scholar 

  • Wikel SK (1999) Tick modulation of host immunity: an important factor in pathogen transmission. Int J Parasitol 29:851–859

    Article  PubMed  CAS  Google Scholar 

  • Woods JA (1988) Lumpy skin disease–a review. Trop Anim Health Prod 20:11–17

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This was a collaborative study between the Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, South Africa and The Pirbright Institute, United Kingdom. The project was funded by the Combating Infectious Diseases of Livestock for International Development (CIDLID) research programme, the Department of International Biotechnology and Biological Sciences Research Council (BBSRC), the UK government, the Department for International Development (DFID) and the Scottish Government (CIDLID project number BB/H009361/1). The authors also thank Professor Albert Mulenga for the guidance on collection of saliva from ticks, Ms Rebone Mahlare and Ms Milana Troskie for their technical assistance and the ARC-OVI for supplying A. hebraeum nymphs and adults.

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Authors and Affiliations

  1. Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, Private bag X04 Onderstepoort, Pretoria, 0110, South Africa

    J. C. Lubinga, W. H. Stoltsz, K. Ebersohn, J. A. W. Coetzer & E. H. Venter

  2. The Pirbright Institute, Pirbright, Surrey, UK

    E. S. M. Tuppurainen

Authors
  1. J. C. Lubinga
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  2. E. S. M. Tuppurainen
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  3. W. H. Stoltsz
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  4. K. Ebersohn
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  5. J. A. W. Coetzer
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  6. E. H. Venter
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Correspondence to J. C. Lubinga.

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Lubinga, J.C., Tuppurainen, E.S.M., Stoltsz, W.H. et al. Detection of lumpy skin disease virus in saliva of ticks fed on lumpy skin disease virus-infected cattle. Exp Appl Acarol 61, 129–138 (2013). https://doi.org/10.1007/s10493-013-9679-5

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  • DOI: https://doi.org/10.1007/s10493-013-9679-5

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