1887

Abstract

Avian pox is a highly contagious avian disease, yet relatively little is known about the epidemiology and transmission of Avipoxviruses. Using a molecular approach, we report evidence for a potential link between birds and field-caught mosquitoes in the transmission of Fowlpox virus (FWPV) in Singapore. Comparison of fpv167 (P4b), fpv126 (VLTF-1), fpv175–176 (A11R-A12L) and fpv140 (H3L) gene sequences revealed close relatedness between FWPV strains obtained from cutaneous lesions of a chicken and four pools of Culex pseudovishnui, Culex spp. (vishnui group) and Coquellitidea crassipes caught in the vicinity of the study site. Chicken-derived viruses characterized during two separate infections two years later were also identical to those detected in the first event, suggesting repeated transmission of closely related FWPV strains in the locality. Since the study location is home to resident and migratory birds, we postulated that wild birds could be the source of FWPV and that bird-biting mosquitoes could act as bridging mechanical vectors. Therefore, we determined whether the FWPV-positive mosquito pools (n=4) were positive for avian DNA using a polymerase chain reaction-sequencing assay. Our findings confirmed the presence of avian host DNA in all mosquito pools, suggesting a role for Cx. pseudovishnui, Culex spp. (vishnui group) and Cq. crassipes mosquitoes in FWPV transmission. Our study exemplifies the utilization of molecular tools to understand transmission networks of pathogens affecting avian populations, which has important implications for the design of effective control measures to minimize disease burden and economic loss.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001209
2019-03-25
2019-12-15
Loading full text...

Full text loading...

/deliver/fulltext/jgv/100/5/838.html?itemId=/content/journal/jgv/10.1099/jgv.0.001209&mimeType=html&fmt=ahah

References

  1. Bolte AL, Meurer J, Kaleta EF. Avian host spectrum of avipoxviruses. Avian Pathol 1999;28:415–432 [CrossRef][PubMed]
    [Google Scholar]
  2. Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA. (editors) Virus Taxonomy: VIIIth Report of the International Committee on Taxonomy of Viruses London: Elsevier Academic Press; 2005
    [Google Scholar]
  3. Zhao K, He W, Xie S, Song D, Lu H et al. Highly pathogenic Fowlpox virus in cutaneously infected chickens, China. Emerg Infect Dis 2014;20:1208–1210 [CrossRef][PubMed]
    [Google Scholar]
  4. Manarolla G, Pisoni G, Sironi G, Rampin T. Molecular biological characterization of avian poxvirus strains isolated from different avian species. Vet Microbiol 2010;140:1–8 [CrossRef][PubMed]
    [Google Scholar]
  5. Kim TJ, Schnitzlein WM, McAloose D, Pessier AP, Tripathy DN. Characterization of an avianpox virus isolated from an Andean condor (Vultur gryphus). Vet Microbiol 2003;96:237–246 [CrossRef][PubMed]
    [Google Scholar]
  6. Hess C, Maegdefrau-Pollan B, Bilic I, Liebhart D, Richter S et al. Outbreak of cutaneous form of poxvirus on a commercial turkey farm caused by the species fowlpox. Avian Dis 2011;55:714–718 [CrossRef][PubMed]
    [Google Scholar]
  7. Tripathy DN, Schnitzlein WM, Morris PJ, Janssen DL, Zuba JK et al. Characterization of poxviruses from forest birds in Hawaii. J Wildl Dis 2000;36:225–230 [CrossRef][PubMed]
    [Google Scholar]
  8. Sadasiv EC, Chang PW, Gulka G. Morphogenesis of canary poxvirus and its entrance into inclusion bodies. Am J Vet Res 1985;46:529–535[PubMed]
    [Google Scholar]
  9. Huw Lee L, Hwa Lee K. Application of the polymerase chain reaction for the diagnosis of fowl poxvirus infection. J Virol Methods 1997;63:113–119 [CrossRef][PubMed]
    [Google Scholar]
  10. Lecis R, Secci F, Antuofermo E, Nuvoli S, Cacciotto C et al. Detection and characterization of an Avipoxvirus in a Common Buzzard (Buteo buteo) in Italy Using a multiple gene approach. J Wildl Dis 2018; [CrossRef][PubMed]
    [Google Scholar]
  11. Ruiz-Martínez J, Ferraguti M, Figuerola J, Martínez-de La Puente J, Williams RA et al. Prevalence and genetic diversity of Avipoxvirus in house sparrows in Spain. PLoS One 2016;11:e0168690 [CrossRef][PubMed]
    [Google Scholar]
  12. Jarmin S, Manvell R, Gough RE, Laidlaw SM, Skinner MA. Avipoxvirus phylogenetics: identification of a PCR length polymorphism that discriminates between the two major clades. J Gen Virol 2006;87:2191–2201 [CrossRef][PubMed]
    [Google Scholar]
  13. Carulei O, Douglass N, Williamson AL. Phylogenetic analysis of three genes of Penguinpox virus corresponding to Vaccinia virus G8R (VLTF-1), A3L (P4b) and H3L reveals that it is most closely related to Turkeypox virus, Ostrichpox virus and Pigeonpox virus. Virol J 2009;6:52 [CrossRef][PubMed]
    [Google Scholar]
  14. Gyuranecz M, Foster JT, Dán Á, Ip HS, Egstad KF et al. Worldwide phylogenetic relationship of avian poxviruses. J Virol 2013;87:4938–4951 [CrossRef][PubMed]
    [Google Scholar]
  15. Afonso CL, Tulman ER, Lu Z, Zsak L, Kutish GF et al. The genome of Fowlpox virus. J Virol 2000;74:3815–3831 [CrossRef][PubMed]
    [Google Scholar]
  16. Tulman ER, Afonso CL, Lu Z, Zsak L, Kutish GF et al. The genome of canarypox virus. J Virol 2004;78:353–366 [CrossRef][PubMed]
    [Google Scholar]
  17. Lüschow D, Hoffmann T, Hafez HM. Differentiation of avian poxvirus strains on the basis of nucleotide sequences of 4b gene fragment. Avian Dis 2004;48:453–462 [CrossRef][PubMed]
    [Google Scholar]
  18. Weli SC, Traavik T, Tryland M, Coucheron DH, Nilssen O. Analysis and comparison of the 4b core protein gene of avipoxviruses from wild birds: evidence for interspecies spatial phylogenetic variation. Arch Virol 2004;149:2035–2046 [CrossRef][PubMed]
    [Google Scholar]
  19. Alley MR, Hale KA, Cash W, Ha HJ, Howe L. Concurrent avian malaria and avipox virus infection in translocated South Island saddlebacks (Philesturnus carunculatus carunculatus). N Z Vet J 2010;58:218–223 [CrossRef][PubMed]
    [Google Scholar]
  20. Aruch S, Atkinson CT, Savage AF, Lapointe DA. Prevalence and distribution of pox-like lesions, avian malaria, and mosquito vectors in Kipahulu Valley, Haleakala National Park, Hawai'i, USA. J Wildl Dis 2007;43:567–575 [CrossRef][PubMed]
    [Google Scholar]
  21. Lapointe DA. Dispersal of Culex quinquefasciatus (Diptera: Culicidae) in a Hawaiian rain forest. J Med Entomol 2008;45:600–609 [CrossRef][PubMed]
    [Google Scholar]
  22. French EL, Reeves WC. A group of viruses isolated from naturally infected mosquitoes collected in the Murray Valley area of Victoria and New South Wales. J Hyg 1954;52:551–562 [CrossRef][PubMed]
    [Google Scholar]
  23. Kligler IJ, Aschner M. Demonstration of presence of Fowl pox Virus in wild caught mosquitoes (Culex Pipiens). Exp Biol Med 1931;28:463–465 [CrossRef]
    [Google Scholar]
  24. Kligler IJ, Muckenfuss RS, Rivers TM. Transmission of Fowl-pox by mosquitoes. J Exp Med 1929;49:649–660 [CrossRef][PubMed]
    [Google Scholar]
  25. Akey BL, Nayar JK, Forrester DJ. Avian pox in Florida wild turkeys: Culex nigripalpus and Wyeomyia vanduzeei as experimental vectors. J Wildl Dis 1981;17:597–599 [CrossRef][PubMed]
    [Google Scholar]
  26. Damassa AJ. The role of culex tarsalis in the transmission of Fowl pox Virus. Avian Dis 1966;10:57–66 [CrossRef]
    [Google Scholar]
  27. Huong CT, Murano T, Uno Y, Usui T, Yamaguchi T. Molecular detection of avian pathogens in poultry red mite (Dermanyssus gallinae) collected in chicken farms. J Vet Med Sci 2014;76:1583–1587 [CrossRef][PubMed]
    [Google Scholar]
  28. Lee HR, Koo BS, Kim JT, Kim HC, Kim MS et al. Molecular epidemiology of avian poxvirus in the oriental turtle dove (Streptopelia orientalis) and the biting midge (Culicoides arakawae) in the Republic of Korea. J Wildl Dis 2017;53:749–760 [CrossRef][PubMed]
    [Google Scholar]
  29. Ergunay K, Gunay F, Oter K, Kasap OE, Orsten S et al. Arboviral surveillance of field-collected mosquitoes reveals circulation of West Nile virus lineage 1 strains in Eastern Thrace, Turkey. Vector Borne Zoonotic Dis 2013;13:744–752 [CrossRef][PubMed]
    [Google Scholar]
  30. Tempelis CH, Lofy MF. A modified precipitin method for identification of mosquito blood-meals *. Am J Trop Med Hyg 1963;12:825–831 [CrossRef]
    [Google Scholar]
  31. Tempelis CH. Host-feeding patterns of mosquitoes, with a review of advances in analysis of blood meals by serology. J Med Entomol 1975;11:635–653 [CrossRef][PubMed]
    [Google Scholar]
  32. Lombardi S, Esposito F. Enzyme-linked immunosorbent assay (ELISA) for the identification of mosquito bloodmeals. Parassitologia 1983;25:49–56[PubMed]
    [Google Scholar]
  33. Edrissian GH, Hafizi A. Application of enzyme-linked immunosorbent assay (ELISA) to identification of Anopheles mosquito bloodmeals. Trans R Soc Trop Med Hyg 1982;76:54–56 [CrossRef][PubMed]
    [Google Scholar]
  34. Burkot TR, Goodman WG, Defoliart GR. Identification of mosquito blood meals by enzyme-linked immunosorbent assay. Am J Trop Med Hyg 1981;30:1336–1341 [CrossRef][PubMed]
    [Google Scholar]
  35. Chow E, Wirtz RA, Scott TW. Identification of blood meals in Aedes aegypti by antibody sandwich enzyme-linked immunosorbent assay. J Am Mosq Control Assoc 1993;9:196–205[PubMed]
    [Google Scholar]
  36. Rurangirwa FR, Minja SH, Musoke AJ, Nantulya VM, Grootenhuis J et al. Production and evaluation of specific antisera against sera of various vertebrate species for identification of bloodmeals of Glossina morsitans centralis. Acta Trop 1986;43:379–389[PubMed]
    [Google Scholar]
  37. Ngo KA, Kramer LD. Identification of mosquito bloodmeals using polymerase chain reaction (PCR) with order-specific primers. J Med Entomol 2003;40:215–222 [CrossRef][PubMed]
    [Google Scholar]
  38. Niare S, Berenger JM, Dieme C, Doumbo O, Raoult D et al. Identification of blood meal sources in the main African malaria mosquito vector by MALDI-TOF MS. Malar J 2016;15:87 [CrossRef][PubMed]
    [Google Scholar]
  39. Townzen JS, Brower AV, Judd DD. Identification of mosquito bloodmeals using mitochondrial cytochrome oxidase subunit I and cytochrome b gene sequences. Med Vet Entomol 2008;22:386–393 [CrossRef][PubMed]
    [Google Scholar]
  40. Bennai K, Tahir D, Lafri I, Bendjaballah-Laliam A, Bitam I et al. Molecular detection of Leishmania infantum DNA and host blood meal identification in Phlebotomus in a hypoendemic focus of human leishmaniasis in northern Algeria. PLoS Negl Trop Dis 2018;12:e0006513 [CrossRef][PubMed]
    [Google Scholar]
  41. Kent RJ, Norris DE. Identification of mammalian blood meals in mosquitoes by a multiplexed polymerase chain reaction targeting cytochrome B. Am J Trop Med Hyg 2005;73:336–342 [CrossRef][PubMed]
    [Google Scholar]
  42. Kent RJ. Molecular methods for arthropod bloodmeal identification and applications to ecological and vector-borne disease studies. Mol Ecol Resour 2009;9:4–18 [CrossRef][PubMed]
    [Google Scholar]
  43. Bram RA. Contributions to the mosquito fauna of Southeast Asia II: the Genus Culex in Thailand (Diptera: Culicidae). Contrib Am Entomol Inst 1967;2:
    [Google Scholar]
  44. Rattanarithikul R, Harrison BA, Panthusiri P, Peyton EL, Coleman RE. Illustrated keys to the mosquitoes of Thailand III. Genera Aedeomyia, Ficalbia, Mimomyia, Hodgesia, Coquillettidia, Mansonia, and Uranotaenia. Southeast Asian J Trop Med Public Health 2006;37:1–85[PubMed]
    [Google Scholar]
  45. Kumar NP, Rajavel AR, Natarajan R, Jambulingam P. DNA barcodes can distinguish species of Indian mosquitoes (Diptera: Culicidae). J Med Entomol 2007;44:1–7 [CrossRef][PubMed]
    [Google Scholar]
  46. Chan A, Chiang LP, Hapuarachchi HC, Tan CH, Pang SC et al. DNA barcoding: complementing morphological identification of mosquito species in Singapore. Parasit Vectors 2014;7:569 [CrossRef][PubMed]
    [Google Scholar]
  47. Versteirt V, Nagy ZT, Roelants P, Denis L, Breman FC et al. Identification of Belgian mosquito species (Diptera: Culicidae) by DNA barcoding. Mol Ecol Resour 2015;15:449–457 [CrossRef][PubMed]
    [Google Scholar]
  48. Wang G, Li C, Guo X, Xing D, Dong Y et al. Identifying the main mosquito species in China based on DNA barcoding. PLoS One 2012;7:e47051 [CrossRef][PubMed]
    [Google Scholar]
  49. Cywinska A, Hunter FF, Hebert PD. Identifying Canadian mosquito species through DNA barcodes. Med Vet Entomol 2006;20:413–424 [CrossRef][PubMed]
    [Google Scholar]
  50. Ashfaq M, Hebert PD, Mirza JH, Khan AM, Zafar Y et al. Analyzing mosquito (Diptera: culicidae) diversity in Pakistan by DNA barcoding. PLoS One 2014;9:e97268 [CrossRef][PubMed]
    [Google Scholar]
  51. Kek R, Hapuarachchi HC, Chung CY, Humaidi MB, Razak MA et al. Feeding host range of Aedes albopictus (Diptera: Culicidae) demonstrates its opportunistic host-seeking behavior in rural Singapore. J Med Entomol 2014;51:880–884 [CrossRef][PubMed]
    [Google Scholar]
  52. Offerman K, Carulei O, Gous TA, Douglass N, Williamson AL. Phylogenetic and histological variation in avipoxviruses isolated in South Africa. J Gen Virol 2013;94:2338–2351 [CrossRef][PubMed]
    [Google Scholar]
  53. Tadese T, Reed WM. Use of restriction fragment length polymorphism, immunoblotting, and polymerase chain reaction in the differentiation of avian poxviruses. J Vet Diagn Invest 2003;15:141–150 [CrossRef][PubMed]
    [Google Scholar]
  54. Lecis R, Secci F, Antuofermo E, Nuvoli S, Scagliarini A et al. Multiple gene typing and phylogeny of avipoxvirus associated with cutaneous lesions in a stone curlew. Vet Res Commun 2017;41:77–83 [CrossRef][PubMed]
    [Google Scholar]
  55. Abdallah FM, Hassanin O. Detection and molecular characterization of avipoxviruses isolated from different avian species in Egypt. Virus Genes 2013;46:63–70 [CrossRef][PubMed]
    [Google Scholar]
  56. Resch W, Weisberg AS, Moss B. Vaccinia virus nonstructural protein encoded by the A11R gene is required for formation of the virion membrane. J Virol 2005;79:6598–6609 [CrossRef][PubMed]
    [Google Scholar]
  57. Yang SJ. Characterization of vaccinia virus A12L protein proteolysis and its participation in virus assembly. Virol J 2007;4:78 [CrossRef][PubMed]
    [Google Scholar]
  58. Laidlaw SM, Skinner MA. Comparison of the genome sequence of FP9, an attenuated, tissue culture-adapted European strain of Fowlpox virus, with those of virulent American and European viruses. J Gen Virol 2004;85:305–322 [CrossRef][PubMed]
    [Google Scholar]
  59. Jarmin SA, Manvell R, Gough RE, Laidlaw SM, Skinner MA. Retention of 1.2 kbp of 'novel' genomic sequence in two European field isolates and some vaccine strains of Fowlpox virus extends open reading frame fpv241. J Gen Virol 2006;87:3545–3549 [CrossRef][PubMed]
    [Google Scholar]
  60. Chathuranga WGD, Karunaratne S, Fernando BR, de Silva W. Diversity, distribution, abundance, and feeding pattern of tropical ornithophilic mosquitoes. J Vector Ecol 2018;43:158–167 [CrossRef][PubMed]
    [Google Scholar]
  61. Njabo KY, Cornel AJ, Sehgal RN, Loiseau C, Buermann W et al. Coquillettidia (Culicidae, Diptera) mosquitoes are natural vectors of avian malaria in Africa. Malar J 2009;8:193 [CrossRef][PubMed]
    [Google Scholar]
  62. Chiang GL, Samarawickrema WA, Eng KL, Cheong WH, Sulaiman I et al. Field studies on the surveillance of Coquillettidia crassipes (Van der Wulp) and the isolation of a strain of Cardiofilaria in peninsular Malaysia. Ann Trop Med Parasitol 1986;80:235–244 [CrossRef][PubMed]
    [Google Scholar]
  63. van Riper C J, Forrester D. Avian pox. 2007;131–176
  64. Thiel T, Whiteman NK, Tirapé A, Baquero MI, Cedeño V et al. Characterization of canarypox-like viruses infecting endemic birds in the Galápagos Islands. J Wildl Dis 2005;41:342–353 [CrossRef][PubMed]
    [Google Scholar]
  65. Ritchie BW. Avian Viruses: Function and Control Lake Worth, Florida: Winger's Publ; 1995; pp.285–311
    [Google Scholar]
  66. Pledger A. Avian pox virus infection in a mourning dove. Can Vet J 2005;46:1143–1145[PubMed]
    [Google Scholar]
  67. Lee JH, Hassan H, Hill G, Cupp EW, Higazi TB et al. Identification of mosquito avian-derived blood meals by polymerase chain reaction-heteroduplex analysis. Am J Trop Med Hyg 2002;66:599–604 [CrossRef][PubMed]
    [Google Scholar]
  68. Mukabana WR, Takken W, Seda P, Killeen GF, Hawley WA et al. Extent of digestion affects the success of amplifying human DNA from blood meals of Anopheles gambiae (Diptera: Culicidae). Bull Entomol Res 2002;92:233–239 [CrossRef][PubMed]
    [Google Scholar]
  69. Siriyasatien P, Pengsakul T, Kittichai V, Phumee A, Kaewsaitiam S et al. Identification of blood meal of field caught Aedes aegypti (L.) by multiplex PCR. Southeast Asian J Trop Med Public Health 2010;41:43–47[PubMed]
    [Google Scholar]
  70. Smits JE, Tella JL, Carrete M, Serrano D, López G. An epizootic of avian pox in endemic short-toed larks (Calandrella rufescens) and Berthelot's pipits (Anthus berthelotti) in the Canary Islands, Spain. Vet Pathol 2005;42:59–65 [CrossRef][PubMed]
    [Google Scholar]
  71. Tripathy DN. The impact of vaccines and the future of genetically modified poxvirus vaccines for poultry. Anim Health Res Rev 2004;5:263–266 [CrossRef][PubMed]
    [Google Scholar]
  72. Khan A, Yousaf A, Khan MZ, Siddique M, Gul ST et al. Cutaneous form of pox infection among captive peafowl (Pavo cristatus) chicks. Avian Pathol 2009;38:65–70 [CrossRef][PubMed]
    [Google Scholar]
  73. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990;215:403–410 [CrossRef][PubMed]
    [Google Scholar]
  74. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994;22:4673–4680 [CrossRef][PubMed]
    [Google Scholar]
  75. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 1999;41:98
    [Google Scholar]
  76. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013;30:2725–2729 [CrossRef][PubMed]
    [Google Scholar]
  77. Posada D. jModelTest: phylogenetic model averaging. Mol Biol Evol 2008;25:1253–1256 [CrossRef][PubMed]
    [Google Scholar]
  78. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003;52:696–704 [CrossRef][PubMed]
    [Google Scholar]
  79. Chapple DG, Ritchie PA. A retrospective approach to testing the DNA barcoding method. PLoS One 2013;8:e77882 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001209
Loading
/content/journal/jgv/10.1099/jgv.0.001209
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error